Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2002 Apr 7;269(1492):665–670. doi: 10.1098/rspb.2001.1911

A possible role for imprinted genes in inbreeding avoidance and dispersal from the natal area in mice.

Anthony R Isles 1, Michael J Baum 1, Dan Ma 1, Abigail Szeto 1, Eric B Keverne 1, Nicholas D Allen 1
PMCID: PMC1690950  PMID: 11934356

Abstract

The expression of a subset of mammalian genes is subject to parent of origin effects (POE), most of which can be explained by genomic imprinting. Analysis of mutant animals has demonstrated that a number of imprinted genes influence brain development and behaviour. Here we provide evidence for POE on olfactory related behaviour and sensitivity to maternal odour cues. This was investigated by examining the odour preference behaviour of reciprocal cross F(1) mice made by embryo transfer to genetically unrelated foster parents. We determined that both adult males and females show an avoidance of female urinary odours of their genetic maternal but not paternal origin. This was found not to be due to any previous exposure to these odours or due to self-learning, but may be related to direct effects on the olfactory system, as reciprocal F(1) males show differential sensitivity to female odour cues. Currently the most robust theory to explain the evolution of imprinting is the conflict hypothesis that focuses on maternal resource allocation to the developing foetus. Kinship considerations are also likely to be important in the selection of imprinted genes and we discuss our findings within this context, suggesting that imprinted genes act directly on the olfactory system to promote post-weaning dispersal from the natal area.

Full Text

The Full Text of this article is available as a PDF (132.6 KB).

Selected References

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

  1. Amadou C., Kumánovics A., Jones E. P., Lambracht-Washington D., Yoshino M., Lindahl K. F. The mouse major histocompatibility complex: some assembly required. Immunol Rev. 1999 Feb;167:211–221. doi: 10.1111/j.1600-065x.1999.tb01394.x. [DOI] [PubMed] [Google Scholar]
  2. Bander S. A., Watson S. C., Shire J. G. Paternal inheritance of egg traits in mice: a case of genomic imprinting. Genet Res. 1989 Dec;54(3):213–219. doi: 10.1017/s0016672300028676. [DOI] [PubMed] [Google Scholar]
  3. Banko M. L., Allen K. M., Dolina S., Neumann P. E., Seyfried T. N. Genomic imprinting and audiogenic seizures in mice. Behav Genet. 1997 Sep;27(5):465–475. doi: 10.1023/a:1025626501148. [DOI] [PubMed] [Google Scholar]
  4. Brambilla R., Gnesutta N., Minichiello L., White G., Roylance A. J., Herron C. E., Ramsey M., Wolfer D. P., Cestari V., Rossi-Arnaud C. A role for the Ras signalling pathway in synaptic transmission and long-term memory. Nature. 1997 Nov 20;390(6657):281–286. doi: 10.1038/36849. [DOI] [PubMed] [Google Scholar]
  5. Burt A., Trivers R. Genetic conflicts in genomic imprinting. Proc Biol Sci. 1998 Dec 22;265(1413):2393–2397. doi: 10.1098/rspb.1998.0589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cattanach B. M., Beechey C. V. Autosomal and X-chromosome imprinting. Dev Suppl. 1990:63–72. [PubMed] [Google Scholar]
  7. Chess A., Simon I., Cedar H., Axel R. Allelic inactivation regulates olfactory receptor gene expression. Cell. 1994 Sep 9;78(5):823–834. doi: 10.1016/s0092-8674(94)90562-2. [DOI] [PubMed] [Google Scholar]
  8. Clutton-Brock T. H. Female transfer and inbreeding avoidance in social mammals. Nature. 1989 Jan 5;337(6202):70–72. doi: 10.1038/337070a0. [DOI] [PubMed] [Google Scholar]
  9. DeChiara T. M., Efstratiadis A., Robertson E. J. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature. 1990 May 3;345(6270):78–80. doi: 10.1038/345078a0. [DOI] [PubMed] [Google Scholar]
  10. Ehlers A., Beck S., Forbes S. A., Trowsdale J., Volz A., Younger R., Ziegler A. MHC-linked olfactory receptor loci exhibit polymorphism and contribute to extended HLA/OR-haplotypes. Genome Res. 2000 Dec;10(12):1968–1978. doi: 10.1101/gr.10.12.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fan W., Liu Y. C., Parimoo S., Weissman S. M. Olfactory receptor-like genes are located in the human major histocompatibility complex. Genomics. 1995 May 1;27(1):119–123. doi: 10.1006/geno.1995.1013. [DOI] [PubMed] [Google Scholar]
  12. Gandon S. Kin competition, the cost of inbreeding and the evolution of dispersal. J Theor Biol. 1999 Oct 21;200(4):345–364. doi: 10.1006/jtbi.1999.0994. [DOI] [PubMed] [Google Scholar]
  13. Gregg B., Thiessen D. D. A simple method of olfactory discrimination of urines for the Mongolian gerbil, Meriones unguiculatus. Physiol Behav. 1981 Jun;26(6):1133–1136. doi: 10.1016/0031-9384(81)90221-3. [DOI] [PubMed] [Google Scholar]
  14. Hurst L. D., McVean G. T. Do we understand the evolution of genomic imprinting? Curr Opin Genet Dev. 1998 Dec;8(6):701–708. doi: 10.1016/s0959-437x(98)80040-3. [DOI] [PubMed] [Google Scholar]
  15. Isles A. R., Baum M. J., Ma D., Keverne E. B., Allen N. D. Urinary odour preferences in mice. Nature. 2001 Feb 15;409(6822):783–784. doi: 10.1038/35057323. [DOI] [PubMed] [Google Scholar]
  16. Isles AR, Wilkinson LS. Imprinted genes, cognition and behaviour. Trends Cogn Sci. 2000 Aug;4(8):309–318. doi: 10.1016/s1364-6613(00)01504-7. [DOI] [PubMed] [Google Scholar]
  17. Keverne E. B., Fundele R., Narasimha M., Barton S. C., Surani M. A. Genomic imprinting and the differential roles of parental genomes in brain development. Brain Res Dev Brain Res. 1996 Mar 29;92(1):91–100. doi: 10.1016/0165-3806(95)00209-x. [DOI] [PubMed] [Google Scholar]
  18. Keverne E. B. Genomic imprinting in the brain. Curr Opin Neurobiol. 1997 Aug;7(4):463–468. doi: 10.1016/s0959-4388(97)80023-2. [DOI] [PubMed] [Google Scholar]
  19. Lau M. M., Stewart C. E., Liu Z., Bhatt H., Rotwein P., Stewart C. L. Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev. 1994 Dec 15;8(24):2953–2963. doi: 10.1101/gad.8.24.2953. [DOI] [PubMed] [Google Scholar]
  20. Lefebvre L., Viville S., Barton S. C., Ishino F., Keverne E. B., Surani M. A. Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest. Nat Genet. 1998 Oct;20(2):163–169. doi: 10.1038/2464. [DOI] [PubMed] [Google Scholar]
  21. Leighton P. A., Ingram R. S., Eggenschwiler J., Efstratiadis A., Tilghman S. M. Disruption of imprinting caused by deletion of the H19 gene region in mice. Nature. 1995 May 4;375(6526):34–39. doi: 10.1038/375034a0. [DOI] [PubMed] [Google Scholar]
  22. Li L., Keverne E. B., Aparicio S. A., Ishino F., Barton S. C., Surani M. A. Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science. 1999 Apr 9;284(5412):330–333. doi: 10.1126/science.284.5412.330. [DOI] [PubMed] [Google Scholar]
  23. Mateo J. M., Johnston R. E. Kin recognition and the 'armpit effect': evidence of self-referent phenotype matching. Proc Biol Sci. 2000 Apr 7;267(1444):695–700. doi: 10.1098/rspb.2000.1058. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McDonald T. P., Jackson C. W. Mode of inheritance of the higher degree of megakaryocyte polyploidization in C3H mice. I. Evidence for a role of genomic imprinting in megakaryocyte polyploidy determination. Blood. 1994 Mar 15;83(6):1493–1498. [PubMed] [Google Scholar]
  25. McGill T. E., Manning A. Genotype and retention of the ejaculatory reflex in castrated male mice. Anim Behav. 1976 Aug;24(3):507–518. doi: 10.1016/s0003-3472(76)80063-2. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Moore T., Haig D. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 1991 Feb;7(2):45–49. doi: 10.1016/0168-9525(91)90230-N. [DOI] [PubMed] [Google Scholar]
  28. Mugford R. A., Nowell N. W. Pheromones and their effect on aggression in mice. Nature. 1970 Jun 6;226(5249):967–968. doi: 10.1038/226967a0. [DOI] [PubMed] [Google Scholar]
  29. O'Shea S. F., Chaure P. T., Halsall J. R., Olesnicky N. S., Leibbrandt A., Connerton I. F., Casselton L. A. A large pheromone and receptor gene complex determines multiple B mating type specificities in Coprinus cinereus. Genetics. 1998 Mar;148(3):1081–1090. doi: 10.1093/genetics/148.3.1081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sundberg H., Døving K., Novikov S., Ursin H. A method for studying responses and habituation to odors in rats. Behav Neural Biol. 1982 Jan;34(1):113–119. doi: 10.1016/s0163-1047(82)91501-1. [DOI] [PubMed] [Google Scholar]
  31. Vogel T., Klose J. Two-dimensional electrophoretic protein patterns of reciprocal hybrids of the mouse strains DBA and C57BL. Biochem Genet. 1992 Dec;30(11-12):649–662. doi: 10.1007/BF02399813. [DOI] [PubMed] [Google Scholar]
  32. 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]

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

RESOURCES