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Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2004 Oct 22;271(1553):2115–2121. doi: 10.1098/rspb.2004.2843

Sex-specific, counteracting responses to inbreeding in a bird.

Tommaso Pizzari 1, Hanne Løvlie 1, Charles K Cornwallis 1
PMCID: PMC1691842  PMID: 15475330

Abstract

Inbreeding often depresses offspring fitness. Because females invest more than males in a reproductive event, inbreeding is expected to be more costly to mothers than fathers, creating a divergence between the reproductive interests of each sex and promoting sex-specific inbreeding strategies. Males and females may bias the probability of inbreeding by selecting copulation partners, and, in sexually promiscuous species, through male strategic sperm investment in different females and female selection of the sperm of different males. However, these processes are often difficult to study, and the way that different male and female strategies interact to determine inbreeding remains poorly understood. Here we demonstrate sex-specific, counteracting responses to inbreeding in the promiscuous red junglefowl, Gallus gallus. First, a male was just as likely to copulate with his full-sib sister as with an unrelated female. In addition, males displayed a tendency to: (i) initiate copulation faster when exposed to an unrelated female than when exposed to a sister, and (ii) inseminate more sperm into sisters than into unrelated females. Second, females retained fewer sperm following insemination by brothers, thus reducing the risk of inbreeding and counteracting male inbreeding strategies.

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Selected References

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  1. Abplanalp H., Sato K., Napolitano D., Reid J. Reproductive performance of inbred congenic Leghorns carrying different haplotypes for the major histocompatibility complex. Poult Sci. 1992 Jan;71(1):9–17. doi: 10.3382/ps.0710009. [DOI] [PubMed] [Google Scholar]
  2. Arnqvist G, Nilsson T. The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav. 2000 Aug;60(2):145–164. doi: 10.1006/anbe.2000.1446. [DOI] [PubMed] [Google Scholar]
  3. Ball M. A., Parker G. A. Sperm competition games: sperm selection by females. J Theor Biol. 2003 Sep 7;224(1):27–42. doi: 10.1016/s0022-5193(03)00118-8. [DOI] [PubMed] [Google Scholar]
  4. Birkhead T. R., Chaline N., Biggins J. D., Burke T., Pizzari T. Nontransitivity of paternity in a bird. Evolution. 2004 Feb;58(2):416–420. [PubMed] [Google Scholar]
  5. Birkhead T. R., Pellatt E. J., Fletcher F. Selection and utilization of spermatozoa in the reproductive tract of the female zebra finch Taeniopygia guttata. J Reprod Fertil. 1993 Nov;99(2):593–600. doi: 10.1530/jrf.0.0990593. [DOI] [PubMed] [Google Scholar]
  6. Birkhead Timothy R., Pizzari Tommaso. Postcopulatory sexual selection. Nat Rev Genet. 2002 Apr;3(4):262–273. doi: 10.1038/nrg774. [DOI] [PubMed] [Google Scholar]
  7. Bretman Amanda, Wedell Nina, Tregenza Tom. Molecular evidence of post-copulatory inbreeding avoidance in the field cricket Gryllus bimaculatus. Proc Biol Sci. 2004 Jan 22;271(1535):159–164. doi: 10.1098/rspb.2003.2563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brillard J. P. Sperm storage and transport following natural mating and artificial insemination. Poult Sci. 1993 May;72(5):923–928. doi: 10.3382/ps.0720923. [DOI] [PubMed] [Google Scholar]
  9. Carlborg Orjan, Kerje Susanne, Schütz Karin, Jacobsson Lina, Jensen Per, Andersson Leif. A global search reveals epistatic interaction between QTL for early growth in the chicken. Genome Res. 2003 Mar;13(3):413–421. doi: 10.1101/gr.528003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chapman T. Seminal fluid-mediated fitness traits in Drosophila. Heredity (Edinb) 2001 Nov;87(Pt 5):511–521. doi: 10.1046/j.1365-2540.2001.00961.x. [DOI] [PubMed] [Google Scholar]
  11. Froman David P., Pizzari Tommaso, Feltmann Allen J., Castillo-Juarez Hector, Birkhead Tim R. Sperm mobility: mechanisms of fertilizing efficiency, genetic variation and phenotypic relationship with male status in the domestic fowl, Gallus gallus domesticus. Proc Biol Sci. 2002 Mar 22;269(1491):607–612. doi: 10.1098/rspb.2001.1925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fumihito A., Miyake T., Takada M., Shingu R., Endo T., Gojobori T., Kondo N., Ohno S. Monophyletic origin and unique dispersal patterns of domestic fowls. Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6792–6795. doi: 10.1073/pnas.93.13.6792. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Garner Trenton W. J., Schmidt Benedikt R. Relatedness, body size and paternity in the alpine newt, Triturus alpestris. Proc Biol Sci. 2003 Mar 22;270(1515):619–624. doi: 10.1098/rspb.2002.2284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kruuk Loeske E. B., Sheldon Ben C., Merilä Juha. Severe inbreeding depression in collared flycatchers (Ficedula albicollis). Proc Biol Sci. 2002 Aug 7;269(1500):1581–1589. doi: 10.1098/rspb.2002.2049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lehmann Laurent, Perrin Nicolas. Inbreeding avoidance through kin recognition: choosy females boost male dispersal. Am Nat. 2003 Nov 6;162(5):638–652. doi: 10.1086/378823. [DOI] [PubMed] [Google Scholar]
  16. Mack Paul D., Hammock Brian A., Promislow Daniel E. L. Sperm competitive ability and genetic relatedness in Drosophila melanogaster: similarity breeds contempt. Evolution. 2002 Sep;56(9):1789–1795. doi: 10.1111/j.0014-3820.2002.tb00192.x. [DOI] [PubMed] [Google Scholar]
  17. Martin-Villa J. M., Longás J., Arnáiz-Villena A. Cyclic expression of HLA class I and II molecules on the surface of purified human spermatozoa and their control by serum inhibin B levels. Biol Reprod. 1999 Dec;61(6):1381–1386. doi: 10.1095/biolreprod61.6.1381. [DOI] [PubMed] [Google Scholar]
  18. Martin P. A., Reimers T. J., Lodge J. R., Dziuk P. J. The effect of ratios and numbers of spermatozoa mixed from two males on proportions of offspring. J Reprod Fertil. 1974 Aug;39(2):251–258. doi: 10.1530/jrf.0.0390251. [DOI] [PubMed] [Google Scholar]
  19. Meagher S., Penn D. J., Potts W. K. Male-male competition magnifies inbreeding depression in wild house mice. Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3324–3329. doi: 10.1073/pnas.060284797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Olsson Mats, Madsen Thomas, Ujvari Beata, Wapstra Erik. Fecundity and MHC affects ejaculation tactics and paternity bias in sand lizards. Evolution. 2004 Apr;58(4):906–909. doi: 10.1111/j.0014-3820.2004.tb00423.x. [DOI] [PubMed] [Google Scholar]
  21. doi: 10.1098/rspb.1997.0010. [DOI] [PMC free article] [Google Scholar]
  22. doi: 10.1098/rspb.1999.0829. [DOI] [PMC free article] [Google Scholar]
  23. Perrin N, Mazalov V., V Local Competition, Inbreeding, and the Evolution of Sex-Biased Dispersal. Am Nat. 2000 Jan;155(1):116–127. doi: 10.1086/303296. [DOI] [PubMed] [Google Scholar]
  24. Pizzari T., Froman D. P., Birkhead T. R. Pre- and post-insemination episodes of sexual selection in the fowl, Gallus g. domesticus. Heredity (Edinb) 2002 Feb;88(2):112–116. doi: 10.1038/sj.hdy.6800014. [DOI] [PubMed] [Google Scholar]
  25. Pizzari Tommaso, Cornwallis Charles K., Løvlie Hanne, Jakobsson Sven, Birkhead Tim R. Sophisticated sperm allocation in male fowl. Nature. 2003 Nov 6;426(6962):70–74. doi: 10.1038/nature02004. [DOI] [PubMed] [Google Scholar]
  26. Reid Jane M., Arcese Peter, Keller Lukas F. Inbreeding depresses immune response in song sparrows (Melospiza melodia): direct and inter-generational effects. Proc Biol Sci. 2003 Oct 22;270(1529):2151–2157. doi: 10.1098/rspb.2003.2480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Steele M. G., Meldrum W., Brillard J. P., Wishart G. J. The interaction of avian spermatozoa with the perivitelline layer in vitro and in vivo. J Reprod Fertil. 1994 Aug;101(3):599–603. doi: 10.1530/jrf.0.1010599. [DOI] [PubMed] [Google Scholar]
  28. Stockley P. Female multiple mating behaviour, early reproductive failure and litter size variation in mammals. Proc Biol Sci. 2003 Feb 7;270(1512):271–278. doi: 10.1098/rspb.2002.2228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Stockley P. No evidence of sperm selection by female common shrews. Proc Biol Sci. 1997 Oct 22;264(1387):1497–1500. doi: 10.1098/rspb.1997.0207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tregenza T., Wedell N. Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol. 2000 Aug;9(8):1013–1027. doi: 10.1046/j.1365-294x.2000.00964.x. [DOI] [PubMed] [Google Scholar]
  31. Tregenza Tom, Wedell Nina. Polyandrous females avoid costs of inbreeding. Nature. 2002 Jan 3;415(6867):71–73. doi: 10.1038/415071a. [DOI] [PubMed] [Google Scholar]
  32. Wishart G. J. Quantitative aspects of sperm:egg interaction in chickens and turkeys. Anim Reprod Sci. 1997 Jul;48(1):81–92. doi: 10.1016/s0378-4320(97)00042-0. [DOI] [PubMed] [Google Scholar]
  33. Wishart G. J. Regulation of the length of the fertile period in the domestic fowl by numbers of oviducal spermatozoa, as reflected by those trapped in laid eggs. J Reprod Fertil. 1987 Jul;80(2):493–498. doi: 10.1530/jrf.0.0800493. [DOI] [PubMed] [Google Scholar]
  34. Zheng W. M., Nishibori M., Isobe N., Yoshimura Y. An in situ hybridization study of the effects of artificial insemination on the localization of cells expressing MHC class II mRNA in the chicken oviduct. Reproduction. 2001 Oct;122(4):581–586. [PubMed] [Google Scholar]
  35. Ziegler Andreas, Dohr Gotrfried, Uchanska-Ziegler Barbara. Possible roles for products of polymorphic MHC and linked olfactory receptor genes during selection processes in reproduction. Am J Reprod Immunol. 2002 Jul;48(1):34–42. doi: 10.1034/j.1600-0897.2002.01097.x. [DOI] [PubMed] [Google Scholar]

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