Skip to main content
PMC home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 1998 Jul 22;265(1403):1299–1306. doi: 10.1098/rspb.1998.0433

MHC-disassortative mating preferences reversed by cross-fostering.

D Penn 1, W Potts 1
PMCID: PMC1689202  PMID: 9718737

Abstract

House mice (Mus musculus domesticus) avoid mating with individuals that are genetically similar at the major histocompatibility complex (MHC). Mice are able recognize MHC-similar individuals through specific odour cues. However, to mate disassortatively for MHC genes, individuals must have a referent, either themselves (self-inspection) or close kin (familial imprinting), with which to compare the MHC identity of potential mates. Although studies on MHC-dependent mating preferences often assume that individuals use self-inspection, laboratory experiments with male mice indicate that they use familial imprinting, i.e. males learn the MHC identity of their family and then avoid mating with females carrying 'familial' MHC alleles. To determine if female mice use familial imprinting, we cross-fostered wild-derived female mouse pups into MHC-dissimilar families, and then tested if this procedure reversed their mating preferences compared with in-fostered controls. Our observations of the female's mating behaviour in seminatural social conditions and the genetic typing of their progeny both indicated that females avoided mating with males carrying MHC genes of their foster family, supporting the familial imprinting hypothesis. We show that MHC-dependent familial imprinting potentially provides a more effective mechanism for avoiding kin matings and reducing inbreeding than self-inspection.

Full Text

The Full Text of this article is available as a PDF (330.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Apanius V., Penn D., Slev P. R., Ruff L. R., Potts W. K. The nature of selection on the major histocompatibility complex. Crit Rev Immunol. 1997;17(2):179–224. doi: 10.1615/critrevimmunol.v17.i2.40. [DOI] [PubMed] [Google Scholar]
  2. Beauchamp G. K., Yamazaki K., Bard J., Boyse E. A. Preweaning experience in the control of mating preferences by genes in the major histocompatibility complex of the mouse. Behav Genet. 1988 Jul;18(4):537–547. doi: 10.1007/BF01065520. [DOI] [PubMed] [Google Scholar]
  3. Buck L. B. Information coding in the vertebrate olfactory system. Annu Rev Neurosci. 1996;19:517–544. doi: 10.1146/annurev.ne.19.030196.002505. [DOI] [PubMed] [Google Scholar]
  4. Eklund A. The effect of early experience on MHC-based mate preferences in two B10.W strains of mice (Mus domesticus). Behav Genet. 1997 May;27(3):223–229. doi: 10.1023/a:1025658013443. [DOI] [PubMed] [Google Scholar]
  5. Estep D. Q., Lanier D. L., Dewsbury D. A. Copulatory behavior and nest building behavior of wild house mice (Mus musculus). Anim Learn Behav. 1975 Nov;3(4):329–336. doi: 10.3758/bf03213455. [DOI] [PubMed] [Google Scholar]
  6. Fillion T. J., Blass E. M. Infantile experience with suckling odors determines adult sexual behavior in male rats. Science. 1986 Feb 14;231(4739):729–731. doi: 10.1126/science.3945807. [DOI] [PubMed] [Google Scholar]
  7. Harvey F. E., Cowley J. J. Effects of external chemical environment on the developing olfactory bulbs of the mouse (Mus musculus). Brain Res Bull. 1984 Oct;13(4):541–547. doi: 10.1016/0361-9230(84)90036-4. [DOI] [PubMed] [Google Scholar]
  8. Hedrick P. W., Black F. L. HLA and mate selection: no evidence in South Amerindians. Am J Hum Genet. 1997 Sep;61(3):505–511. doi: 10.1086/515519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Manning C. J., Wakeland E. K., Potts W. K. Communal nesting patterns in mice implicate MHC genes in kin recognition. Nature. 1992 Dec 10;360(6404):581–583. doi: 10.1038/360581a0. [DOI] [PubMed] [Google Scholar]
  10. Ober C., Weitkamp L. R., Cox N., Dytch H., Kostyu D., Elias S. HLA and mate choice in humans. Am J Hum Genet. 1997 Sep;61(3):497–504. doi: 10.1086/515511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Penn D., Potts W. How do major histocompatibility complex genes influence odor and mating preferences? Adv Immunol. 1998;69:411–436. doi: 10.1016/s0065-2776(08)60612-4. [DOI] [PubMed] [Google Scholar]
  12. Porter R. H., Moore J. D. Human kin recognition by olfactory cues. Physiol Behav. 1981 Sep;27(3):493–495. doi: 10.1016/0031-9384(81)90337-1. [DOI] [PubMed] [Google Scholar]
  13. Potts W. K., Manning C. J., Wakeland E. K. Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature. 1991 Aug 15;352(6336):619–621. doi: 10.1038/352619a0. [DOI] [PubMed] [Google Scholar]
  14. Potts W. K., Manning C. J., Wakeland E. K. The role of infectious disease, inbreeding and mating preferences in maintaining MHC genetic diversity: an experimental test. Philos Trans R Soc Lond B Biol Sci. 1994 Nov 29;346(1317):369–378. doi: 10.1098/rstb.1994.0154. [DOI] [PubMed] [Google Scholar]
  15. Potts W. K., Wakeland E. K. Evolution of MHC genetic diversity: a tale of incest, pestilence and sexual preference. Trends Genet. 1993 Dec;9(12):408–412. doi: 10.1016/0168-9525(93)90103-o. [DOI] [PubMed] [Google Scholar]
  16. Saha B. K., Cullen S. E. Molecular mapping of murine I region recombinants: crossing over in the E beta gene. J Immunol. 1986 Feb 1;136(3):1112–1116. [PubMed] [Google Scholar]
  17. Sullivan Regina M., Wilson Donald A., Leon Michael. Associative Processes in Early Olfactory Preference Acquisition: Neural and Behavioral Consequences. Psychobiology (Austin, Tex) 1989;17(1):29–33. doi: 10.3758/bf03337814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Terry L. M., Johanson I. B. Effects of altered olfactory experiences on the development of infant rats' responses to odors. Dev Psychobiol. 1996 May;29(4):353–377. doi: 10.1002/(SICI)1098-2302(199605)29:4<353::AID-DEV4>3.0.CO;2-P. [DOI] [PubMed] [Google Scholar]
  19. Wang H. W., Wysocki C. J., Gold G. H. Induction of olfactory receptor sensitivity in mice. Science. 1993 May 14;260(5110):998–1000. doi: 10.1126/science.8493539. [DOI] [PubMed] [Google Scholar]
  20. Wedekind C., Füri S. Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity? Proc Biol Sci. 1997 Oct 22;264(1387):1471–1479. doi: 10.1098/rspb.1997.0204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Wedekind C. Mate choice and maternal selection for specific parasite resistances before; during and after fertilization. Philos Trans R Soc Lond B Biol Sci. 1994 Nov 29;346(1317):303–311. doi: 10.1098/rstb.1994.0147. [DOI] [PubMed] [Google Scholar]
  22. Wedekind C., Seebeck T., Bettens F., Paepke A. J. MHC-dependent mate preferences in humans. Proc Biol Sci. 1995 Jun 22;260(1359):245–249. doi: 10.1098/rspb.1995.0087. [DOI] [PubMed] [Google Scholar]
  23. Woo C. C., Coopersmith R., Leon M. Localized changes in olfactory bulb morphology associated with early olfactory learning. J Comp Neurol. 1987 Sep 1;263(1):113–125. doi: 10.1002/cne.902630110. [DOI] [PubMed] [Google Scholar]
  24. Yamazaki K., Beauchamp G. K., Kupniewski D., Bard J., Thomas L., Boyse E. A. Familial imprinting determines H-2 selective mating preferences. Science. 1988 Jun 3;240(4857):1331–1332. doi: 10.1126/science.3375818. [DOI] [PubMed] [Google Scholar]
  25. Yamazaki K., Boyse E. A., Miké V., Thaler H. T., Mathieson B. J., Abbott J., Boyse J., Zayas Z. A., Thomas L. Control of mating preferences in mice by genes in the major histocompatibility complex. J Exp Med. 1976 Nov 2;144(5):1324–1335. doi: 10.1084/jem.144.5.1324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yamazaki K., Yamaguchi M., Baranoski L., Bard J., Boyse E. A., Thomas L. Recognition among mice. Evidence from the use of a Y-maze differentially scented by congenic mice of different major histocompatibility types. J Exp Med. 1979 Oct 1;150(4):755–760. doi: 10.1084/jem.150.4.755. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES