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Evolutionary Ecology

, Volume 21, Issue 5, pp 687–702 | Cite as

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

  • Aditi Pai
  • Stacy Feil
  • Guiyun Yan
Original Paper

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.

Keywords

Tribolium castaneum Fitness Polyandry Male–female co-evolution 

Notes

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.

References

  1. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  2. 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 268:399–405CrossRefGoogle Scholar
  3. Arnaud L, Haubruge E, Gage MJG (2001) Sperm size and number variation in the red flour beetle. Zool J Linn Soc 133:369–375CrossRefGoogle Scholar
  4. Arnqvist G, Edvardsson M, Friberg U, Nilsson T (2000) Sexual conflict promotes speciation in insects. P Natl Acad Sci USA 97:10460–10464CrossRefGoogle Scholar
  5. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164PubMedCrossRefGoogle Scholar
  6. Arnqvist G, Rowe L (2002) Antagonistic coevolution between the sexes in a group of insects. Nature 415:787–789PubMedGoogle Scholar
  7. Attia FA,Tregenza T (2004) Divergence revealed by population crosses in the red flour beetle Tribolium castaneum. Evol Ecol Res 6:927–935Google Scholar
  8. Baer B, Schmid-Hempel P (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397:151–154CrossRefGoogle Scholar
  9. Baer B, Schmid-Hempel P (2001) Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. Evolution 55:1639–1643PubMedGoogle Scholar
  10. 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 143:417–426PubMedGoogle Scholar
  11. Beeman R, Brown S (1999) RAPD-based genetic linkage maps of Tribolium castaenum. Genetics 153:333–338PubMedGoogle Scholar
  12. Bernasconi G, Keller L (2001) Female polyandry affects son’s reproductive success in the red flour beetle Tribolium castaneum. J Evol Biol 14:186–193CrossRefGoogle Scholar
  13. Birkhead T (2000) Promiscuity: an evolutionary history of sperm competition. Harvard University, CambridgeGoogle Scholar
  14. Boake C, Wade M (1984) Populations of red flour beetle Tribolium castaneum (Coleoptera: Tenebrionidae) differ in their sensitivity to aggregation pheromones. Environ Entomol 13:1182–1185Google Scholar
  15. Boughman JW (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944–948PubMedCrossRefGoogle Scholar
  16. Brooker M, Rowley I, Adams M, Baverstock P (1990) Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species? Behav Ecol Sociobiol 26:191–199Google Scholar
  17. Brown DV, Eady PE (2001) Functional incompatibility between the fertilization systems of two allopatric populations of Callosobruchus maculatus (Coleoptera: Bruchidae). Evolution 55:2257–2262PubMedGoogle Scholar
  18. Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Tr Ecol Evol 18:41–47CrossRefGoogle Scholar
  19. Clark A, Begun D, Prout T (1999) Female X male interactions in Drosophila sperm competition. Science 283:217–220PubMedCrossRefGoogle Scholar
  20. 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 291–370Google Scholar
  21. 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 54:2161–2165PubMedGoogle Scholar
  22. Eberhard W (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, PrincetonGoogle Scholar
  23. Endler JA, Houde AE (1995) Geographic variation in female preferences for male traits in Poecilia reticulata. Evolution 49:456–468CrossRefGoogle Scholar
  24. Evans JP, Magurran AE (2000) Multiple benefits of multiple mating in guppies. P Natl Acad Sci USA 97:10074–10076CrossRefGoogle Scholar
  25. Gavrilets S, Arnqvist G, Friberg U (2001) The evolution of female mate choice by sexual conflict. Proc Roy Soc Lond B 268:531–539CrossRefGoogle Scholar
  26. 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 255:159–165CrossRefGoogle Scholar
  27. Gray DA, Cade WH (2000) Sexual selection and speciation in field crickets. P Natl Acad Sci USA 97:14449–14454CrossRefGoogle Scholar
  28. Harano T, Miyatake T (2005) Heritable variation in polyandry in Callosobruchus chinensis. Anim Behav 70:299–304CrossRefGoogle Scholar
  29. Härdling R, Kaitala A (2005) The evolution of repeated mating under sexual conflict. J Evol Biol 18:106–115PubMedCrossRefGoogle Scholar
  30. Holland B, Rice W (1999) Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes reproductive load. P Natl Acad Sci USA 96:5083–5088CrossRefGoogle Scholar
  31. Hosken DJ, Garner TWJ, Ward PI (2001) Sexual conflict selects for male and female reproductive characters. Curr Biol 11:489–493PubMedCrossRefGoogle Scholar
  32. Jennions M, Petrie M (1997) Variation in mate choice and mating preferences: a review of causes and consequences. Biol Rev 72:283–327PubMedCrossRefGoogle Scholar
  33. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64PubMedCrossRefGoogle Scholar
  34. Konior M, Radwan J, Kolodziejczyk M (2001) Polyandry increases offspring fecundity in the bulb mite. Evolution 55:1893–1896PubMedGoogle Scholar
  35. Kwiatkowski MA, Sullivan BK (2002) Geographic variation in sexual selection among populations of an iguanid lizard, Sauromalus obesus (=ater). Evolution 56:2039–2051PubMedGoogle Scholar
  36. Lesna I, Sabelis MW (1999) Diet-dependent female choice for males with `good genes’ in a soil predatory mite. Nature 401:581–584CrossRefGoogle Scholar
  37. 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 255:31–36CrossRefGoogle Scholar
  38. Masta SE, Maddison WP (2002) Sexual selection driving diversification in jumping spiders. P Natl Acad Sci USA 99:4442–4447CrossRefGoogle Scholar
  39. Nilsson T, Fricke C, Arnqvist G (2002) Patterns of divergence in the effects of mating on female reproductive performance in flour beetles. Evolution 56:111–120PubMedGoogle Scholar
  40. 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 53:227–233CrossRefGoogle Scholar
  41. Olsson M, Madsen T, Shine R, Gullberg A, Tegelstrom H (1994) Rewards of promiscuity. Nature 372:229–230CrossRefGoogle Scholar
  42. Olsson M, Shine R, Madsen T, Gullberg A, Tegelstrom H (1996) Sperm selection by females. Nature 383:585CrossRefGoogle Scholar
  43. Orsetti DM, Rutowski RL (2003) No material benefits, and a fertilization cost, for multiple mating by female leaf beetles. Anim Behav 66:477–484CrossRefGoogle Scholar
  44. Pai A, Yan G (2002a) Polyandry produces sexy sons at the cost of daughters in red flour beetles. Proc Roy Soc Lond B 269:361–368CrossRefGoogle Scholar
  45. Pai A, Yan G (2002b) Female mate choice in relation to heterozygosity in Tribolium castaneum. J Evol Biol 15:1076–1082CrossRefGoogle Scholar
  46. Pai A, Yan G (2003) Rapid female multiple mating in red flour beetles (Tribolium castaneum). Can J Zoo 81:888–896CrossRefGoogle Scholar
  47. Pai A, Bennett L, Yan G (2005) Female multiple mating for fertility assurance in red flour beetles? Can J Zool 83:913–919CrossRefGoogle Scholar
  48. Parker GA, Partridge L (1998) Sexual conflict and speciation. Philos T Roy Soc B 353:261–274CrossRefGoogle Scholar
  49. Rice WR (1996) Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381:232–234PubMedCrossRefGoogle Scholar
  50. Ridley M (1988) Mating frequency and fecundity in insects. Biol Rev Cambr Phil Soc 63:509–549Google Scholar
  51. SAS (1995) JMP statistics and graphics guide. SAS Institute, CaryGoogle Scholar
  52. 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 254:173–179CrossRefGoogle Scholar
  53. 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 98:6709–6713CrossRefGoogle Scholar
  54. Uy JAC, Borgia G (2000) Sexual selection drives rapid divergence in bowerbird display traits. Evolution 54:273–278PubMedGoogle Scholar
  55. Wade MJ (1977) An experimental study of group selection. Evolution 31:134–153CrossRefGoogle Scholar
  56. 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 92:2519–2523CrossRefGoogle Scholar
  57. Yan G, Stevens L (1995) Selection by parasites on components of fitness in Tribolium beetles: the effect of intraspecific competition. Am Nat 146:795–813CrossRefGoogle Scholar
  58. Zeh JA, Zeh DW (1996) The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc Roy Soc Lond B 263:1711–1717CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  1. 1.Biology DepartmentSpelman CollegeAtlantaUSA
  2. 2.Department of Biological SciencesState University of New York at BuffaloBuffaloUSA
  3. 3.School of Biological SciencesUniversity of California IrvineIrvineUSA

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