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Variation in polyandry and its fitness consequences among populations of the red flour beetle, Tribolium castaneum

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Abstract

Female mating with multiple males in a single reproductive period, or polyandry, is a common phenomenon in animals. In this study we investigated variation in female mating behavior and its fitness consequences among three genetic strains of the red flour beetle, Tribolium castaneum. We found that the extent of polyandry and its fitness consequences varied significantly among the strains. In the first strain PRUZ, females mated multiply but incurred costs of polyandry in the form of reduced offspring production. Females of the second strain, NDG11, mated readily with multiple partners and benefited because polyandry led to higher offspring quality. Finally, TIW1 females were resistant to multiple mating and polyandry resulted in lower offspring production but improved offspring quality. Thus, in the first population we observed only costs of polyandry, in the second strain only benefits of polyandry whereas in the third we detected both costs and benefits of polyandry. Possible explanations for such a pattern are discussed.

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References

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Andres JA, Arnqvist G (2001) Genetic divergence of the seminal signal-receptor system in houseflies: the footprints of sexually antagonistic coevolution? Proc Roy Soc Lond B 268:399–405

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Arnqvist G, Edvardsson M, Friberg U, Nilsson T (2000) Sexual conflict promotes speciation in insects. P Natl Acad Sci USA 97:10460–10464

    Article  CAS  Google Scholar 

  • Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164

    Article  PubMed  Google Scholar 

  • Arnqvist G, Rowe L (2002) Antagonistic coevolution between the sexes in a group of insects. Nature 415:787–789

    PubMed  CAS  Google Scholar 

  • Attia FA,Tregenza T (2004) Divergence revealed by population crosses in the red flour beetle Tribolium castaneum. Evol Ecol Res 6:927–935

    Google Scholar 

  • Baer B, Schmid-Hempel P (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397:151–154

    Article  CAS  Google Scholar 

  • Baer B, Schmid-Hempel P (2001) Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. Evolution 55:1639–1643

    PubMed  CAS  Google Scholar 

  • Beeman RW, Thomson MS, Clark JM, DeCamillis MA, Brown SJ, Denell RE (1996) Woot, an active gypsy-class retrotransposon in the flour beetle, Tribolium castaneum, is associated with a recent mutation. Genetics 143:417–426

    PubMed  CAS  Google Scholar 

  • Beeman R, Brown S (1999) RAPD-based genetic linkage maps of Tribolium castaenum. Genetics 153:333–338

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Birkhead T (2000) Promiscuity: an evolutionary history of sperm competition. Harvard University, Cambridge

    Google Scholar 

  • Boake C, Wade M (1984) Populations of red flour beetle Tribolium castaneum (Coleoptera: Tenebrionidae) differ in their sensitivity to aggregation pheromones. Environ Entomol 13:1182–1185

    Google Scholar 

  • Boughman JW (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944–948

    Article  PubMed  CAS  Google Scholar 

  • Brooker M, Rowley I, Adams M, Baverstock P (1990) Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species? Behav Ecol Sociobiol 26:191–199

    Google Scholar 

  • Brown DV, Eady PE (2001) Functional incompatibility between the fertilization systems of two allopatric populations of Callosobruchus maculatus (Coleoptera: Bruchidae). Evolution 55:2257–2262

    PubMed  CAS  Google Scholar 

  • Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Tr Ecol Evol 18:41–47

    Article  Google Scholar 

  • Clark A, Begun D, Prout T (1999) Female X male interactions in Drosophila sperm competition. Science 283:217–220

    Article  PubMed  CAS  Google Scholar 

  • Drummond B (1984) Multiple mating and sperm competition in the Lepidoptera. In: Smith RL (ed) Sperm competition and the evolution of animal mating strategies. Academic Press Orlando, FL, pp 291–370

    Google Scholar 

  • Eady PE, Wilson N, Jackson M (2000) Copulating with multiple mates enhances female fecundity but not egg-to-adult survival in the bruchid beetle Callosobruchus maculatus. Evolution 54:2161–2165

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Endler JA, Houde AE (1995) Geographic variation in female preferences for male traits in Poecilia reticulata. Evolution 49:456–468

    Article  Google Scholar 

  • Evans JP, Magurran AE (2000) Multiple benefits of multiple mating in guppies. P Natl Acad Sci USA 97:10074–10076

    Article  CAS  Google Scholar 

  • Gavrilets S, Arnqvist G, Friberg U (2001) The evolution of female mate choice by sexual conflict. Proc Roy Soc Lond B 268:531–539

    Article  CAS  Google Scholar 

  • Gilburn A, Day T (1994) Evolution of female choice in seaweed flies: fisherian and good genes mechanisms operate in different populations. Proc Roy Soc Lond B 255:159–165

    Article  Google Scholar 

  • Gray DA, Cade WH (2000) Sexual selection and speciation in field crickets. P Natl Acad Sci USA 97:14449–14454

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Härdling R, Kaitala A (2005) The evolution of repeated mating under sexual conflict. J Evol Biol 18:106–115

    Article  PubMed  Google Scholar 

  • Holland B, Rice W (1999) Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes reproductive load. P Natl Acad Sci USA 96:5083–5088

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jennions M, Petrie M (1997) Variation in mate choice and mating preferences: a review of causes and consequences. Biol Rev 72:283–327

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Konior M, Radwan J, Kolodziejczyk M (2001) Polyandry increases offspring fecundity in the bulb mite. Evolution 55:1893–1896

    PubMed  CAS  Google Scholar 

  • Kwiatkowski MA, Sullivan BK (2002) Geographic variation in sexual selection among populations of an iguanid lizard, Sauromalus obesus (=ater). Evolution 56:2039–2051

    PubMed  Google Scholar 

  • Lesna I, Sabelis MW (1999) Diet-dependent female choice for males with `good genes’ in a soil predatory mite. Nature 401:581–584

    Article  CAS  Google Scholar 

  • Magurran AE, Seghers BH (1994) Sexual conflict as a consequence of ecology: evidence from Guppy, Poecilia reticulata, populations in Trinidad. Proc Roy Soc Lond B 255:31–36

    Article  Google Scholar 

  • Masta SE, Maddison WP (2002) Sexual selection driving diversification in jumping spiders. P Natl Acad Sci USA 99:4442–4447

    Article  CAS  Google Scholar 

  • Nilsson T, Fricke C, Arnqvist G (2002) Patterns of divergence in the effects of mating on female reproductive performance in flour beetles. Evolution 56:111–120

    PubMed  Google Scholar 

  • Nilsson T, Fricke C, Arnqvist G (2003) The effects of male and female genotype on variance in male fertilization success in the red flour beetle (Tribolium castaneum). Behav Ecol Sociobiol 53:227–233

    Article  Google Scholar 

  • Olsson M, Madsen T, Shine R, Gullberg A, Tegelstrom H (1994) Rewards of promiscuity. Nature 372:229–230

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Orsetti DM, Rutowski RL (2003) No material benefits, and a fertilization cost, for multiple mating by female leaf beetles. Anim Behav 66:477–484

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Pai A, Yan G (2002b) Female mate choice in relation to heterozygosity in Tribolium castaneum. J Evol Biol 15:1076–1082

    Article  Google Scholar 

  • Pai A, Yan G (2003) Rapid female multiple mating in red flour beetles (Tribolium castaneum). Can J Zoo 81:888–896

    Article  Google Scholar 

  • Pai A, Bennett L, Yan G (2005) Female multiple mating for fertility assurance in red flour beetles? Can J Zool 83:913–919

    Article  Google Scholar 

  • Parker GA, Partridge L (1998) Sexual conflict and speciation. Philos T Roy Soc B 353:261–274

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ridley M (1988) Mating frequency and fecundity in insects. Biol Rev Cambr Phil Soc 63:509–549

    Google Scholar 

  • SAS (1995) JMP statistics and graphics guide. SAS Institute, Cary

    Google Scholar 

  • Stockley P, Searle JB, MacDonald DW, Jones CS (1993) Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding. Proc Roy Soc Lond B 254:173–179

    Article  CAS  Google Scholar 

  • Ting C-T, Takahashi A, Wu C-I (2001) Incipient speciation by sexual isolation in Drosophila: concurrent evolution at multiple loci. P Natl Acad Sci USA 98:6709–6713

    Article  CAS  Google Scholar 

  • Uy JAC, Borgia G (2000) Sexual selection drives rapid divergence in bowerbird display traits. Evolution 54:273–278

    PubMed  CAS  Google Scholar 

  • Wade MJ (1977) An experimental study of group selection. Evolution 31:134–153

    Article  Google Scholar 

  • Wu C, Hollocher H, Begun D, Aquadaro C, Xu Y, Wu M (1995) Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation. P Natl Acad Sci USA 92:2519–2523

    Article  CAS  Google Scholar 

  • Yan G, Stevens L (1995) Selection by parasites on components of fitness in Tribolium beetles: the effect of intraspecific competition. Am Nat 146:795–813

    Article  Google Scholar 

  • Zeh JA, Zeh DW (1996) The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc Roy Soc Lond B 263:1711–1717

    Article  Google Scholar 

Download references

Acknowledgments

We thank C. Kane, T. Cottom, G. Bajwa, M. Park, and K. Tran for technical assistance. A. Monteiro and anonymous reviewers provided useful suggestions on improving the manuscript. The research is supported by National Science Foundation grant IBN 1030165. These experiments comply with the current laws of the country they were conducted in.

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Author notes

  1. Aditi Pai

    Present address: Biology Department, Spelman College, 280 Science Center, Atlanta, GA, 30314, USA

  2. Guiyun Yan

    Present address: School of Biological Sciences, University of California Irvine, 3038 Hewitt Hall, Irvine, CA, 92697, USA

Authors and Affiliations

  1. Department of Biological Sciences, State University of New York at Buffalo, 220 Hochstetter Hall, Buffalo, 14260, NY, USA

    Aditi Pai, Stacy Feil & Guiyun Yan

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  1. Aditi Pai
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Correspondence to Aditi Pai.

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Pai, A., Feil, S. & Yan, G. Variation in polyandry and its fitness consequences among populations of the red flour beetle, Tribolium castaneum . Evol Ecol 21, 687–702 (2007). https://doi.org/10.1007/s10682-006-9146-4

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