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Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 1998 Nov 7;265(1410):2087–2093. doi: 10.1098/rspb.1998.0544

Maternal effects on the development of social rank and immunity trade-offs in male laboratory mice (Mus musculus).

C J Barnard 1, J M Behnke 1, A R Gage 1, H Brown 1, P R Smithurst 1
PMCID: PMC1689489  PMID: 9842735

Abstract

Social status in randomly constituted groups of male CFLP mice was predictable from early suckling behaviour and rate of weight gain in natal litters. High-ranking males were those that had suckled on more anterior teats and gained weight more quickly. Rank was not predicted by any measures of sibling interaction or hormone (testosterone, corticosterone) concentration. Aggressiveness in eventual high-rankers was associated negatively with the proportion of males in the litter at birth and the amount of maternal attention received. Aggressive social relationships within natal litters did not predict polarized rank relationships in randomized groups. Nevertheless, while still in their natal litters, and in the absence of aggressive rank relationships, eventual rank categories showed the same difference in modulation of testosterone concentration in relation to current immunocompetence (low-rankers modulating, high-rankers not), as has repeatedly been found in randomized groups by earlier studies. The role of maternal condition in determining rank-related life-history development in male mice is discussed.

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Selected References

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  1. Barker D. J. The fetal and infant origins of disease. Eur J Clin Invest. 1995 Jul;25(7):457–463. doi: 10.1111/j.1365-2362.1995.tb01730.x. [DOI] [PubMed] [Google Scholar]
  2. Barker D. J. The fetal origins of hypertension. J Hypertens Suppl. 1996 Dec;14(5):S117–S120. [PubMed] [Google Scholar]
  3. Barnard C. J., Behnke J. M., Gage A. R., Brown H., Smithurst P. R. Immunity costs and behavioural modulation in male laboratory mice (Mus musculus) exposed to the odours of females. Physiol Behav. 1997 Oct;62(4):857–866. doi: 10.1016/s0031-9384(97)00249-7. [DOI] [PubMed] [Google Scholar]
  4. Barnard C. J., Behnke J. M., Gage A. R., Brown H., Smithurst P. R. Modulation of behaviour and testosterone concentration in immunodepressed male laboratory mice (Mus musculus). Physiol Behav. 1997 Jun;61(6):907–917. doi: 10.1016/s0031-9384(97)00011-5. [DOI] [PubMed] [Google Scholar]
  5. Barnard C. J., Behnke J. M., Gage A. R., Brown H., Smithurst P. R. The role of parasite-induced immunodepression, rank and social environment in the modulation of behaviour and hormone concentration in male laboratory mice (Mus musculus). Proc Biol Sci. 1998 Apr 22;265(1397):693–701. doi: 10.1098/rspb.1998.0349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Barnard C. J., Behnke J. M., Sewell J. Environmental enrichment, immunocompetence, and resistance to Babesia microti in male mice. Physiol Behav. 1996 Nov;60(5):1223–1231. doi: 10.1016/s0031-9384(96)00174-6. [DOI] [PubMed] [Google Scholar]
  7. Barnard C. J., Behnke J. M., Sewell J. Social behaviour and susceptibility to infection in house mice (Mus musculus): effects of group size, aggressive behaviour and status-related hormonal responses prior to infection on resistance to Babesia microti. Parasitology. 1994 Jun;108(Pt 5):487–496. doi: 10.1017/s0031182000077349. [DOI] [PubMed] [Google Scholar]
  8. Barnard C. J., Behnke J. M., Sewell J. Social behaviour, stress and susceptibility to infection in house mice (Mus musculus): effects of duration of grouping and aggressive behaviour prior to infection on susceptibility to Babesia microti. Parasitology. 1993 Aug;107(Pt 2):183–192. doi: 10.1017/s0031182000067299. [DOI] [PubMed] [Google Scholar]
  9. Behnke J. M., Barnard C. J., Wakelin D. Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. Int J Parasitol. 1992 Nov;22(7):861–907. doi: 10.1016/0020-7519(92)90046-n. [DOI] [PubMed] [Google Scholar]
  10. Clark P. M., Hindmarsh P. C., Shiell A. W., Law C. M., Honour J. W., Barker D. J. Size at birth and adrenocortical function in childhood. Clin Endocrinol (Oxf) 1996 Dec;45(6):721–726. doi: 10.1046/j.1365-2265.1996.8560864.x. [DOI] [PubMed] [Google Scholar]
  11. Clutton-Brock T. H., Iason G. R. Sex ratio variation in mammals. Q Rev Biol. 1986 Sep;61(3):339–374. doi: 10.1086/415033. [DOI] [PubMed] [Google Scholar]
  12. Cresswell J. L., Egger P., Fall C. H., Osmond C., Fraser R. B., Barker D. J. Is the age of menopause determined in-utero? Early Hum Dev. 1997 Sep 19;49(2):143–148. doi: 10.1016/s0378-3782(97)00028-5. [DOI] [PubMed] [Google Scholar]
  13. Freeland W. J. Parasitism and behavioral dominance among male mice. Science. 1981 Jul 24;213(4506):461–462. doi: 10.1126/science.7244643. [DOI] [PubMed] [Google Scholar]
  14. Gandelman R., vom Saal F. S., Reinisch J. M. Contiguity to male foetuses affects morphology and behaviour of female mice. Nature. 1977 Apr 21;266(5604):722–724. doi: 10.1038/266722a0. [DOI] [PubMed] [Google Scholar]
  15. Haig D. Genetic conflicts in human pregnancy. Q Rev Biol. 1993 Dec;68(4):495–532. doi: 10.1086/418300. [DOI] [PubMed] [Google Scholar]
  16. Hales C. N. Metabolic consequences of intrauterine growth retardation. Acta Paediatr Suppl. 1997 Nov;423:184–188. doi: 10.1111/j.1651-2227.1997.tb18410.x. [DOI] [PubMed] [Google Scholar]
  17. Hoy S., Lutter C., Puppe B., Wähner M. Zusammenhänge zwischen der Vitalität neugeborener Ferkel, der Saugordnung, Mortalität und der Lebendmasseentwicklung bis zum Absetzen. Berl Munch Tierarztl Wochenschr. 1995 Jun;108(6):224–228. [PubMed] [Google Scholar]
  18. Langley-Evans S. Fetal programming of immune function and respiratory disease. Clin Exp Allergy. 1997 Dec;27(12):1377–1379. [PubMed] [Google Scholar]
  19. Lucion A. B., De-Almeida R. M., Da-Silva R. S. Territorial aggression, body weight, carbohydrate metabolism and testosterone levels of wild rats maintained in laboratory colonies. Braz J Med Biol Res. 1996 Dec;29(12):1657–1662. [PubMed] [Google Scholar]
  20. Namikas J., Wehmer F. Gender composition of the litter affects behavior of male mice. Behav Biol. 1978 Jun;23(2):219–224. doi: 10.1016/s0091-6773(78)91830-8. [DOI] [PubMed] [Google Scholar]
  21. Palanza P., Parmigiani S., vom Saal F. S. Urine marking and maternal aggression of wild female mice in relation to anogenital distance at birth. Physiol Behav. 1995 Nov;58(5):827–835. doi: 10.1016/0031-9384(95)00107-t. [DOI] [PubMed] [Google Scholar]
  22. Phillips D. I. Insulin resistance as a programmed response to fetal undernutrition. Diabetologia. 1996 Sep;39(9):1119–1122. doi: 10.1007/BF00400663. [DOI] [PubMed] [Google Scholar]
  23. Rohner-Jeanrenaud E., Jeanrenaud B. Central nervous system and body weight regulation. Ann Endocrinol (Paris) 1997;58(2):137–142. [PubMed] [Google Scholar]
  24. Trivers R. L., Willard D. E. Natural selection of parental ability to vary the sex ratio of offspring. Science. 1973 Jan 5;179(4068):90–92. doi: 10.1126/science.179.4068.90. [DOI] [PubMed] [Google Scholar]
  25. Virgin C. E., Jr, Sapolsky R. M. Styles of male social behavior and their endocrine correlates among low-ranking baboons. Am J Primatol. 1997;42(1):25–39. doi: 10.1002/(SICI)1098-2345(1997)42:1<25::AID-AJP2>3.0.CO;2-0. [DOI] [PubMed] [Google Scholar]

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