Skip to main content
Log in

The genetic basis of traits regulating sperm competition and polyandry: can selection favour the evolution of good- and sexy-sperm?

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The good-sperm and sexy-sperm (GS-SS) hypotheses predict that female multiple mating (polyandry) can fuel sexual selection for heritable male traits that promote success in sperm competition. A major prediction generated by these models, therefore, is that polyandry will benefit females indirectly via their sons’ enhanced fertilization success. Furthermore, like classic ‘good genes’ and ‘sexy son’ models for the evolution of female preferences, GS-SS processes predict a genetic correlation between genes for female mating frequency (analogous to the female preference) and those for traits influencing fertilization success (the sexually selected traits). We examine the premise for these predictions by exploring the genetic basis of traits thought to influence fertilization success and female mating frequency. We also highlight recent debates that stress the possible genetic constraints to evolution of traits influencing fertilization success via GS-SS processes, including sex-linked inheritance, nonadditive effects, interacting parental genotypes, and trade-offs between integrated ejaculate components. Despite these possible constraints, the available data suggest that male traits involved in sperm competition typically exhibit substantial additive genetic variance and rapid evolutionary responses to selection. Nevertheless, the limited data on the genetic variation in female mating frequency implicate strong genetic maternal effects, including X-linkage, which is inconsistent with GS-SS processes. Although the relative paucity of studies on the genetic basis of polyandry does not allow us to draw firm conclusions about the evolutionary origins of this trait, the emerging pattern of sex linkage in genes for polyandry is more consistent with an evolutionary history of antagonistic selection over mating frequency. We advocate further development of GS-SS theory to take account of the complex evolutionary dynamics imposed by sexual conflict over mating frequency.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anderson MJ, Dixson AF (2002) Motility and the midpiece in primates. Nature 416:496

    PubMed  CAS  Google Scholar 

  • Arnaud L, Haubruge E, Gage MJG (2001) Sperm size and number variation in the red flour beetle. Zoo J Linnean Soc 133:369–375

    Article  Google Scholar 

  • Arnqvist G (1998) Comparative evidence for the evolution of genitalia by sexual selection. Nature 393:784–786

    CAS  Google Scholar 

  • Arnqvist G, Danielsson I (1999) Copulatory behavior, genital morphology, and male fertilization success in water striders. Evolution 53:147–156

    Google Scholar 

  • Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, New Jersey

    Google Scholar 

  • Arnqvist G, Thornhill R (1998) Evolution of animal genitalia: patterns of phenotypic and genotypic variation and condition dependence of genital and non-genital morphology in water strider (Heteroptera: Gerridae: Insecta). Genet Res 71:193–212

    Google Scholar 

  • Baer B, Schmid-Hempel P, Hoeg JT, Boomsma JJ (2003) Sperm length, sperm storage and mating system characteristics in bumblebees. Insectes Sociaux 50:101–108

    Google Scholar 

  • Balshine S, Leach BJ, Neat F, Werner NY, Montgomerie R (2001) Sperm size of African cichlids in relation to sperm competition. Behav Ecol 12:726–731

    Google Scholar 

  • Bernasconi G, Keller L (2001) Female polyandry affects their sons’ reproductive success in the red flour beetle Tribolium castaneum. J Evol Biol 14:186–193

    Google Scholar 

  • Birkhead TR, Chaline N, Biggins JD, Burke T, Pizzari T (2004) Nontransitivity of paternity in a bird. Evolution 58:416–420

    PubMed  CAS  Google Scholar 

  • Birkhead TR, Martínez JG, Burke T, Froman DP (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc Roy Soc Lond B 266:1759–1764

    CAS  Google Scholar 

  • Birkhead TR, Pellatt EJ, Brekke P, Yeates R, Castillo-Juarez H (2005) Genetic effects on sperm design in the zebra finch. Nature 434:383–387

    PubMed  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Blanckenhorn WU, Hellriegel B, Hosken DJ, Jann P, Altwegg R, Ward PI (2004) Does testis size track expected mating success in yellow dung flies? Funct Ecol 18:414–418

    Google Scholar 

  • Briskie JV, Montgomerie R (1992) Sperm size and sperm competition in birds. Proc Roy Soc Lond B 247:89–95

    CAS  Google Scholar 

  • Byrne PG, Simmons LW, Roberts JD (2003) Sperm competition and the evolution of gamete morphology in frogs. Proc Roy Soc Lond B 270:2079–2086

    Google Scholar 

  • Cameron E, Day T, Rowe L (2003) Sexual conflict and indirect benefits. J Evol Biol 16:1055–1060

    PubMed  CAS  Google Scholar 

  • Casselman SJ, Montgomerie R (2004) Sperm traits in relation to male quality in colonial spawning bluegill. J Fish Biol 64:1700–1711

    Google Scholar 

  • Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L (1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:241–244

    PubMed  CAS  Google Scholar 

  • Clark AG (2002) Sperm competition and the maintenance of polymorphism. Heredity 88:148–153

    PubMed  CAS  Google Scholar 

  • Clark AG, Aguade M, Prout T, Harshman LG, Langley CH (1995) Variation in sperm displacement and its association with accessory-gland protein loci in Drosophila melanogaster. Genetics 139:189–201

    PubMed  CAS  Google Scholar 

  • Clark AG, Begun DJ (1998) Female genotypes affect sperm displacement in Drosophila. Genetics 149:1487–1493

    PubMed  CAS  Google Scholar 

  • Clark AG, Begun DJ, Prout T (1999) Female × male interactions in Drosophila sperm competition. Science 283:217–220

    PubMed  CAS  Google Scholar 

  • Crnokrak P, Roff DA (1995) Dominance variance—associations with selection and fitness. Heredity 75:530–540

    Google Scholar 

  • Curtsinger JW (1991) Sperm competition and the evolution of multiple mating. Am Nat 138:93–102

    Google Scholar 

  • Danielsson I, Askenmo C (1999) Male genital traits and mating interval affect male fertilization success in the water strider Gerris lacustris. Behav Ecol Sociobiol 46:149–156

    Google Scholar 

  • Dowling DK, Nowostawski AL, Arnqvist G (2006) Effects of cytoplasmic genes on sperm viability and sperm morphology in a seed beetle: implications for sperm competition theory? J Evol Biol 20:358–368

    Google Scholar 

  • Droney DC (1998) The influence of the nutritional content of the adult male diet on testis mass, body condition and courtship vigour in a Hawaiian Drosophila. Funct Ecol 12:920–928

    Google Scholar 

  • Eady PE (1995) Why do male Callosobruchus maculatus beetles inseminate so many sperm? Behav Ecol Sociobiol 36:25–32

    Google Scholar 

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

    Google Scholar 

  • Eberhard WG, Cordero C (2003) Sexual conflict and female choice. Trends Ecol Evol 18:438–439

    Google Scholar 

  • Engqvist L, Sauer KP (2001) Strategic male mating effort and cryptic male choice in a scorpionfly. Proc Roy Soc Lond B 268:729–735

    CAS  Google Scholar 

  • Engqvist L, Sauer KP (2003) Determinants of sperm transfer in the scorpionfly Panorpa cognata: male variation, female condition and copulation duration. J Evol Biol 16:1196–1204

    PubMed  CAS  Google Scholar 

  • Evans JP, Marshall DJ (2005) Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution 59:106–112

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Evans MR, Goldsmith AR (2000) Male wrens with large testes breed early. Anim Behav 60:101–105

    PubMed  Google Scholar 

  • Fairbairn DJ, Vermette R, Kapoor NN, Zahiri N (2003) Functional morphology of sexually selected gentalia in the water strider Aquarius remigis. Can J Zoo 81:400–413

    Google Scholar 

  • Fisher DO, Double MC, Blomberg SP, Jennions MD, Cockburn A (2006) Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild. Nature 444:89–92

    PubMed  CAS  Google Scholar 

  • Fiumera AC, Dumont BL, Clark AG (2005) Sperm competitive ability in Drosophila melanogaster associated with variation in male reproductive proteins. Genetics 169:243–257

    PubMed  CAS  Google Scholar 

  • Friberg U, Lew TA, Byrne PG, Rice WR (2005) Assessing the potential for an ongoing arms race within and between the sexes: selection and heritable variation. Evolution 59:1540–1551

    PubMed  Google Scholar 

  • Froman DP, Kirby JD (2005) Sperm mobility: phenotype in roosters (Gallus domesticus) determined by mitochondrial function. Biol Reprod 72:562–567

    PubMed  CAS  Google Scholar 

  • Froman DP, Pizzari T, Feltmann AJ, Castillo-Juarez H, Birkhead TR (2002) Sperm mobility: mechanisms of fertilizing efficiency, genetic variation and phenotypic relationship with male status in the domestic fowl, Gallus gallus domesticus. Proc Roy Soc Lond B 269:607–612

    Google Scholar 

  • Gage MJG (1994) Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proc Roy Soc Lond B 258:247–254

    Google Scholar 

  • Gage MJG (1995) Continuous variation in reproductive strategy as an adaptive response to population density in the moth Plodia interpunctella. Proc Roy Soc Lond B 261:25–30

    Google Scholar 

  • 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 Roy Soc Lond B 270:625–632

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Gage MJG, Morrow EH (2003) Experimental evidence for the evolution of numerous, tiny sperm via sperm competition. Curr Biol 13:754–757

    PubMed  CAS  Google Scholar 

  • Gallon F, Marchetti C, Jouy N, Marchetti P (2006) The functionality of mitochondria differentiates human spermatozoa with high and low fertilizing capability. Fertil Steril 86:1526–1530

    PubMed  Google Scholar 

  • García-González F, Simmons LW (2005) Sperm viability matters in insect sperm competition. Curr Biol 15:271–275

    PubMed  Google Scholar 

  • García-González F, Simmons LW (2007) Shorter sperm confer higher competitive fertilization success. Evolution 61:816–824

    PubMed  Google Scholar 

  • Gemmell NJ, Metcalf VJ, Allendorf FW (2004) Mother’s curse: the effect of mtDNA on individual fitness and population viability. Trends Ecol Evol 19:238–244

    PubMed  Google Scholar 

  • Gibson JR, Chippindale AK, Rice WR (2002) The X chromosome is a hot spot for sexually antagonistic fitness variation. Proc Roy Soc Lond B 269:499–505

    Google Scholar 

  • Gomendio M, Coello-Martin J, Crespo C, Magaña C, Roldan ERS (2006) Sperm competition enhances functional capacity of mammalian spermatozoa. Proc Nat Acad Sci USA 203:15113–15117

    Google Scholar 

  • Gomendio M, Harcourt AH, Roldan ERS (1998) Sperm competition in mammals. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, San Diego, pp 667–751

    Google Scholar 

  • Gomendio M, Roldan ERS (1991) Sperm competition influences sperm size in mammals. Proc Roy Soc Lond B 243:181–185

    CAS  Google Scholar 

  • Gromko MH, Newport MEA (1988) Genetic basis for remating in Drosophila melanogaster.II. Response to selection based on the behavior of one sex. Behav Gene 18:621–632

    CAS  Google Scholar 

  • Gustafsson L (1986) Lifetime reproductive success and heritability: empirical support for Fisher’s fundamental theorem. Am Nat 128:761–764

    Google Scholar 

  • Harano T, Miyatake T (2005) Heritable variation in polyandry in Callosobruchus chinensis. Anim Behav 70:299–304

    Google Scholar 

  • Harcourt AH (1991) Sperm competition and the evolution of nonfertilizing sperm in mammals. Evolution 45:314–328

    Google Scholar 

  • Harcourt AH, Purvis A, Liles L (1995) Sperm competition: mating system, not breeding season, affects testes size of primates. Funct Ecol 9:468–476

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hettyey A, Roberts JD (2006) Sperm traits of the quacking frog, Crinia georgiana: intra- and interpopulation variation in a species with a high risk of sperm competition. Behav Ecol Sociobiol 59:389–396

    Google Scholar 

  • Holleley CE, Dickman CR, Crowther MS, Oldroyd BP (2006) Size breeds success: multiple paternity, multivariate selection and male semelparity in a small marsupial, Antechinus stuartii. Mol Ecol 15:3439–3448

    PubMed  CAS  Google Scholar 

  • Hosken DJ (1997) Sperm competition in bats. Proc Roy Soc Lond B 264:385–392

    CAS  Google Scholar 

  • Hosken DJ, Garner TWJ, Blanckenhorn WU (2003) Asymmetry, testis and sperm size in yellow dung flies. Funct Ecol 17:231–236

    Google Scholar 

  • Hosken DJ, Garner TWJ, Tregenza T, Wedell N, Ward PI (2003) Superior sperm competitors sire higher-quality young. Proc Roy Soc Lond B 270:1933–1938

    CAS  Google Scholar 

  • Hosken DJ, Garner TWJ, Ward PI (2001) Sexual conflict selects for male and female reproductive characters. Curr Biol 11:489–493

    PubMed  CAS  Google Scholar 

  • Hosken DJ, Stockley P (2004) Sexual selection and genital evolution. Trends Ecol Evol 19:87–93

    PubMed  Google Scholar 

  • House CM, Simmons LW (2005) The evolution of male genitalia: patterns of genetic variation and covariation in the genital sclerites of the dung beetle Onthophagus taurus. J Evol Biol 18:1281–2192

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Hughes KA (1997) Quantitative genetics of sperm precedence in Drosophila melanogaster. Genetics 145:139–151

    PubMed  CAS  Google Scholar 

  • Hunter FM, Birkhead TR (2002) Sperm viability and sperm competition in insects. Curr Biol 12:121–123

    PubMed  CAS  Google Scholar 

  • Immler S, Moore HDM, Breed WG, Birkhead TR (2007) By hook or by crook? Morphometry, competition and cooperation in roden sperm. Plos One 1:e170

    Google Scholar 

  • Iwasa Y, Pomiankowski A, Nee S (1991) The evolution of costly mate preferences II. The “handicap” principle. Evolution 45:1431–1442

    Google Scholar 

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

    PubMed  CAS  Google Scholar 

  • Johnson DDP, Briskie JV (1999) Sperm competition and sperm length in shorebirds. Condor 101:848–854

    Google Scholar 

  • Joly D, Korol A, Nevo E (2004) Sperm size evolution in Drosophila: inter- and intraspecific analysis. Genetica 120:233–244

    PubMed  Google Scholar 

  • Keller L, Reeve HK (1995) Why do females mate with multiple males? The sexually selected sperm hypothesis. Adv Study Anim Behav 24:291–315

    Article  Google Scholar 

  • Konior M, Keller L, Radwan J (2005) Effect of inbreeding and heritability of sperm competition success in the bulb mite Rhizoglyphus robini. Heredity 94:577–581

    PubMed  CAS  Google Scholar 

  • Konior M, Radwan J, Kolodziejczyk M, Keller L (2006) Strong association between a single gene and fertilization efficiency of males and fecundity of their mates in the bulb mite. Proc Roy Soc Lond B 273:309–314

    CAS  Google Scholar 

  • Kraus FB, Neumann P, Moritz RFA (2005) Genetic variance of mating frequency in the honeybee (Apis mellifera L.). Insectes Sociaux 52:1–5

    Google Scholar 

  • LaMunyon CW, Ward S (1998) Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proc Roy Soc Lond B 265:1997–2002

    CAS  Google Scholar 

  • Langerhans RB, Layman CA, DeWitt TJ (2005) Male genital size reflects a tradeoff between attracting mates and avoiding predators in two live-bearing fish species. Proc Nat Acad Sci USA 102:7618–7623

    PubMed  CAS  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Google Scholar 

  • Lewis SM, Austad SN (1990) Sources of intraspecific variation in sperm precedence in red flour beetles. Am Nat 135:351–359

    Google Scholar 

  • Linhart O, Rodina M, Gela D, Kocour M, Vandeputte M (2005) Spermatozoal competition in common carp (Cyprinus carpio): what is the primary determinant of competition success? Reproduction 130:705–711

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Inc, Sunderland

    Google Scholar 

  • Malo AF, Gomendio M, Garde J, Lang-Lenton B, Soler AJ, Roldan ERS (2006) Sperm design and sperm function. Biol Lett 2:246–249

    PubMed  Google Scholar 

  • Malo AF, Roldan ERS, Garde J, Soler AJ, Gomendio M (2005) Antlers honestly advertise sperm production and quality. Proc Roy Soc Lond B 272:149–157

    Google Scholar 

  • Marshall DJ, Evans JP (2005) The benefits of polyandry in the free-spawning polychaete Galeolaria caespitosa. J Evol Biol 18:735–741

    PubMed  CAS  Google Scholar 

  • Merilä J, Sheldon BC (1999) Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity 83:103–109

    PubMed  Google Scholar 

  • Merilä J, Sheldon BC (1999) Testis size variation in the greenfinch Carduelis chloris: relevance for some recent models of sexual selection. Behav Ecol Sociobiol 45:115–123

    Google Scholar 

  • Merilä J, Sheldon BC (2000) Lifetime reproductive success and heritability in nature. Am Nat 155:301–310

    PubMed  Google Scholar 

  • Miller GT, Pitnick S (2002) Sperm-female coevolution in Drosophila. Science 298:1230–1233

    PubMed  CAS  Google Scholar 

  • Minoretti N, Baur B (2006) Among- and within-population variation in sperm quality in the simultaneously hermaphroditic land snail Arianta arbustorum. Behav Ecol Sociobiol 60:270–280

    Google Scholar 

  • Miyatake T, Matsumura F (2004) Intra-specific variation in female remating in Callosobruchus chinensis and C. maculatus. J Insect Physiol 50:403–408

    PubMed  CAS  Google Scholar 

  • Moore AJ, Gowaty PA, Wallin WG, Moore PJ (2001) Sexual conflict and the evolution of female mate choice and male social dominance. Proc Roy Soc Lond B 268:517–523

    CAS  Google Scholar 

  • Moore FL, Reijo-Pera RA (2000) Male sperm motility dictated by mother’s mtDNA. Am J Hum Genet 67:543–548

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Morrow EH, Gage MJG (2000) The evolution of sperm length in moths. Proc Roy Soc Lond B 267:307–313

    CAS  Google Scholar 

  • Morrow EH, Gage MJG (2001) Artificial selection and heritability of sperm length in Gryllus bimaculatus. Heredity 87:356–362

    PubMed  CAS  Google Scholar 

  • Morrow EH, Gage MJG (2001) Consistent significant variation between individual males in spermatozoal morphology. J Zoo 254:147–153

    Google Scholar 

  • Morrow EH, Gage MJG (2001) Sperm competition experiments between lines of crickets producing different sperm lengths. Proc Roy Soc Lond B 268:2281–2286

    CAS  Google Scholar 

  • Nakada K, Sato A, Yoshida K, Morita T, Tanaka H, Inoue SI, Yonekawa H, Hayashi JI (2006) Mitochondria-related male infertility. Proc Nat Acad Sci USA 103:15148–15153

    PubMed  CAS  Google Scholar 

  • Neff BD, Fu P, Gross MR (2003) Sperm investment and alternative mating tactics in bluegill sunfish (Lepomis macrochirus). Behav Ecol 14:634–641

    Google Scholar 

  • Oppliger A, Naciri-Graven Y, Ribi G, Hosken DJ (2003) Sperm length influences fertilization success during sperm competition in the snail Viviparus ater. Mol Ecol 12:485–492

    PubMed  CAS  Google Scholar 

  • Pai AT, Yan GY (2002) Polyandry produces sexy sons at the cost of daughters in red flour beetles. Proc Roy Soc Lond B 269:361–368

    Google Scholar 

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

    Google Scholar 

  • Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic Press, New York, pp 123–166

    Google Scholar 

  • Parker GA (1982) Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J Theor Biol 96:281–294

    PubMed  CAS  Google Scholar 

  • Pattarini JA, Starmer WT, Bjork A, Pitnick S (2006) Mechanisms underlying the sperm quality advantage in Drosophila melanogaster. Evolution 60:2064–2080

    PubMed  Google Scholar 

  • Pischedda A, Chippindale AK (2006) Intralocus sexual conflict diminishes the benefits of sexual selection. Plos Biol 4:2099–2103

    CAS  Google Scholar 

  • Pitcher TE, Dunn PO, Whittingham LA (2005) Sperm competition and the evolution of testes size in birds. J Evol Biol 18:557–567

    PubMed  CAS  Google Scholar 

  • Pitcher TE, Rodd FH, Rowe L (2007) Sexual colouration and sperm traits in guppies. J Fish Biol 70:165–177

    Google Scholar 

  • Pitnick S, Miller GT (2000) Correlated response in reproductive and life history traits to selection on testis length in Drosophila hydei. Heredity 84:416–426

    PubMed  Google Scholar 

  • Pitnick S, Miller GT, Reagan J, Holland B (2001) Males' evolutionary responses to experimental removal of sexual selection. Proc Roy Soc Lond B 268:1071–1080

    CAS  Google Scholar 

  • Pizzari T, Birkhead TR (2002) The sexually-selected sperm hypothesis: sex-biased inheritance and sexual antagonism. Biol Rev 77:183–209

    PubMed  CAS  Google Scholar 

  • Pomiankowski A, Iwasa Y, Nee S (1991) The evolution of costly mate preferences I. Fisher and biased mutation. Evolution 45:1422–1430

    Google Scholar 

  • Preston BT, Stevenson IR, Pemberton JM, Coltman DW, Wilson K (2003) Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proc Roy Soc Lond B 270:633–640

    CAS  Google Scholar 

  • Preziosi RF, Fairbairn DJ (2000) Lifetime selection on adult body size and components of body size in a waterstrider: opposing selection and maintenance of sexual size dimorphism. Evolution 54:558–566

    PubMed  CAS  Google Scholar 

  • Pyle DW, Gromko MH (1979) Genetic basis for repeated mating in Drosophila melanogaster. Am Nat 117:133–146

    Google Scholar 

  • Radwan J (1996) Intraspecific variation in sperm competition success in the bulb mite: a role for sperm size. Proc Roy Soc Lond B 263:855–859

    Google Scholar 

  • Radwan J (1998) Heritability of sperm competition success in the bulb mite, Rhizoglyphus robini. J Evol Biol 11:321–327

    Google Scholar 

  • Rakitin A, Ferguson MM, Trippel EA (1999) Sperm competition and fertilization success in Atlantic cod (Gadus morhua): effect of sire size and condition factor on gamete quality. Can J Fish Aqua Sci 56:2315–2323

    Google Scholar 

  • Ramm SA, Parker GA, Stockley P (2005) Sperm competition and the evolution of male reproductive anatomy in rodents. Proc Roy Soc Lond B 272:949–955

    Google Scholar 

  • Reeve HK, Pfennig DW (2003) Genetic biases for showy males: are some genetic systems especially conducive to sexual selection? Proc Nat Acad Sci USA 100:1089–1094

    PubMed  CAS  Google Scholar 

  • Reinhardt K (2001) Determinants of ejaculate size in a grasshopper (Chorthippus parallelus). Behav Ecol Sociobiol 50:503–510

    Google Scholar 

  • Rice WR (1984) Sex chromosomes and the evolution of sexual dimorphism. Evolution 38:735–742

    Google Scholar 

  • Rice WR (1996) Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381:232–234

    PubMed  CAS  Google Scholar 

  • Rice WR, Chippindale AK (2001) Intersexual ontogenetic conflict. J Evol Biol 14:685–693

    Google Scholar 

  • Rice WR, Holland B (1997) The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behav Ecol Sociobiol 41:1–10

    Google Scholar 

  • Roff DA, Emerson K (2006) Epistasis and dominance: evidence for differential effects in life-history versus morphological traits. Evolution 60:1981–1990

    PubMed  Google Scholar 

  • Rowe L, Houle D (1996) The lek paradox and the capture of genetic variance by condition dependent traits. Proc Roy Soc Lond B 263:1415–1421

    Google Scholar 

  • Schulte-Hostedde AI, Millar JS (2004) Intraspecific variation of testis size and sperm length in the yellow-pine chipmunk (Tamias amoenus): implications for sperm competition and reproductive success. Behav Ecol Sociobiol 55:272–277

    Google Scholar 

  • Schulte-Hostedde AI, Millar JS, Hickling GJ (2003) Intraspecific variation in testis size of small mammals: implications for muscle mass. Can J Zoo 81:591–595

    Google Scholar 

  • Schulte-Hostedde AI, Millar JS, Hickling GJ (2005) Condition dependence of testis size in small mammals. Evol Ecol Res 7:143–149

    Google Scholar 

  • Schulte-Hostedde AI, Montgomerie R (2006) Intraspecific variation in ejaculate traits of the northern watersnake (Nerodia sipedon). J Zoo 270:147–152

    Google Scholar 

  • Sgro CM, Chapman T, Partridge L (1998) Sex-specific selection on time to remate in Drosophila melanogaster. Anim Behav 56:1267–1278

    PubMed  Google Scholar 

  • Shuker DM, Phillimore AJ, Burton-Chellew MN, Hodge SE, West SA (2007) The quantitative genetic basis of polyandry in the parasitoid wasp, Nasonia vitripennis. Heredity 98:69–73

    PubMed  CAS  Google Scholar 

  • Simmons LW (2003) The evolution of polyandry: patterns of genotypic variation in female mating frequency, male fertilization success and a test of the sexy-sperm hypothesis. J Evol Biol 16:624–634

    PubMed  CAS  Google Scholar 

  • Simmons LW (2005) The evolution of polyandry: sperm competition, sperm selection and offspring viability. Ann Rev Ecol Evol Systemat 36:125–146

    Google Scholar 

  • Simmons LW, Kotiaho JS (2002) Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution 56:1622–1631

    PubMed  Google Scholar 

  • Simmons LW, Moore AJ (2007) Evolutionary quantitative genetics of sperm. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm evolution (in press)

  • Simmons LW, Tomkins JL, Hunt J (1999) Sperm competition games played by dimorphic male beetles. Proc Roy Soc Lond B 266:145–150

    Google Scholar 

  • Simmons LW, Wernham J, Garcia-Gonzalez 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

    Google Scholar 

  • Singh SR, Singh BN (2001) Female remating in Drosophila ananassae: bidirectional selection for remating speed. Behav Genet 31:361–370

    PubMed  CAS  Google Scholar 

  • Sivinski J (1984) Sperm in competition. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems, pp 85–115

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

    PubMed  Google Scholar 

  • Solymar BD, Wade WH (1990) Heritable variation for female mating frequency in field crickets, Gryllus integer. Behav Ecol Sociobiol 26:73–76

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Stockley P, Searle JB, Macdonald DW, Jones CS (1994) Alternative reproductive tactics in male common shrews—relationships between mate searching behavior, sperm production, and reproductive success as revealed by DNA fingerprinting. Behav Ecol Sociobiol 34:71–78

    Google Scholar 

  • Thornhill R (1983) Cryptic female choice and its implications in the scorpionfly Harpobittacus nigricepts. Am Nat 122:765–788

    Google Scholar 

  • Tomkins JL, Radwan J, Kotiaho JS, Tregenza T (2004) Genic capture and resolving the lek paradox. Trends Ecol Evol 19:323–328

    PubMed  Google Scholar 

  • Torres-Vila LM, Gragera J, Rodriguez-Molina MC, Stockel J (2002) Heritable variation for female remating in Lobesia botrana, a usually monandrous moth. Anim Behav 64:899–907

    Google Scholar 

  • Torres-Vila LM, Rodriguez-Molina MC, Gragera J, Bielza-Lino P (2001) Polyandry in Lepidoptera: a heritable trait in Spodoptera exigua Hubner. Heredity 86:177–183

    PubMed  CAS  Google Scholar 

  • Ward PI (1998) Intraspecific variation in sperm size characters. Heredity 80:655–659

    PubMed  Google Scholar 

  • Ward PI (2000) Sperm length is heritable and sex-linked in the yellow dung fly (Scathophaga stercoraria). J Zool 251:349–353

    Google Scholar 

  • Wedell N (2001) Female remating in butterflies: interaction between female genotype and nonfertile sperm. J Evol Biol 14:746–754

    Google Scholar 

  • Wedell N, Wiklund C, Cook PA (2002) Monandry and polyandry as alternative lifestyles in a butterfly. Behav Ecol 13:450–455

    Google Scholar 

  • Wenninger EJ, Averill AL (2006) Influence of body and genital morphology on relative male fertilization success in oriental beetle. Behav Ecol 17:656–663

    Google Scholar 

  • Werner M, Simmons LW (2007) The evolution of male genitalia: functional integration of genital sclerites in the dung beetle Onthophagus taurus. Biol J Linnean Soc (in press)

  • Wilson N, Tubman SC, Eady PE, Robertson GW (1997) Female genotype affects male success in sperm competition. Proc Roy Soc Lond B 264:1491–1495

    Google Scholar 

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

    Google Scholar 

  • Zeh JA (2004) Sexy sons: a dead end for cytoplasmic genes. Proc Roy Soc Lond B 271:S306–S309

    CAS  Google Scholar 

  • Zeh JA, Zeh DW (2005) Maternal inheritance, sexual conflict and the maladapted male. Trends Genet 21:281–286

    PubMed  CAS  Google Scholar 

  • Zeng ZB, Liu JJ, Stam LF, Kao CH, Mercer JM, Laurie CC (2000) Genetic architecture of a morphological shape difference between two Drosophila species. Genetics 154:299–310

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to members of the Centre for Evolutionary Biology at UWA, and Janne Kotiaho and John Bridle for discussion, and Trevor Pitcher and Herman Mays for organising the Symposium on the Evolutionary Ecology of Genetic Quality (Tours, France, 2006), which provided the impetus for this contribution. JPE and LWS are funded by the Australian Research Council.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jonathan P. Evans.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Evans, J.P., Simmons, L.W. The genetic basis of traits regulating sperm competition and polyandry: can selection favour the evolution of good- and sexy-sperm?. Genetica 134, 5–19 (2008). https://doi.org/10.1007/s10709-007-9162-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-007-9162-5

Keywords

Navigation