Female behaviour plays a critical role in controlling murine pregnancy block

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1662, 2009, Pages 1723-1729

  Becker, Stuart D ^a   Hurst, Jane L ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Behaviour; Bruce effect; Mouse; Pregnancy block; Reproduction; Rodent

Indexed keywords

BEHAVIORAL RESPONSE; FEMALE BEHAVIOR; ODOR; PREGNANCY; REPRODUCTION; RODENT;

ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; FEMALE; MALE; MOUSE; NONHUMAN; ODOR; PREGNANCY; PRIORITY JOURNAL; PROGENY; REPRODUCTION; SEXUAL SELECTION; SOCIAL BEHAVIOR; SOCIAL STATUS; SURVIVAL;

MURINAE; MUS; RODENTIA;

ANIMALS; BEHAVIOR, ANIMAL; FEMALE; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PREGNANCY; PREGNANCY, ANIMAL; REPRODUCTION; SEX ATTRACTANTS; SOCIAL DOMINANCE;

EID: 66349102276     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.1780     Document Type: Article

References (51)

1. ASAB/ABS 2006 Guidelines for the treatment of animals in behavioural research and teaching. Anim. Behav. 71, 245-253.
2. Barkley, M. S., Bradford, G. E. & Geschwind, I. I. 1978 Pattern of plasma prolactin concentration during first half of mouse gestation. Biol. Reprod. 19, 291-296.
3. Becker, S. D. & Hurst, J. L. 2008 Pregnancy block from a female perspective. In Chemical signals in vertebrates 11 (eds J. L. Hurst, R. J. Beynon, S. C. Roberts & T. D. Wyatt), pp. 141-150. New York, NY: Springer.
4. Bellringer, J. F., Pratt, H. P. M. & Keverne, E. B. 1980 Involvement of the vomeronasal organ and prolactin in pheromonal induction of delayed implantation in mice. J. Reprod. Fertil. 59, 223-228.
5. Brennan, P. A. & Peele, P. 2003 Towards an understanding of the pregnancy-blocking urinary chemosignals of mice. Biochem. Soc. Trans. 31, 152-155.
6. Brennan, P., Kaba, H. & Keverne, E. B. 1990 Olfactory recognition: a simple memory system. Science 250, 1223-1226. (Pubitemid 120031829)
7. Bronson, F. H. & Coquelin, A. 1980 The modulation of reproduction by priming pheromones in house mice: speculations on adaptive function. In Chemical signals: vertebrates and aquatic invertebrates (eds D. Müller-Schwartze & R. M. Silverstein), pp. 243-265. New York, NY: Plenum.
8. Bruce, H. M. 1959 An exteroceptive block to pregnancy in the mouse. Nature 184, 105.
9. Bruce, H. M. 1960 A block to pregnancy in the mouse caused by proximity of strange males. J. Reprod. Fertil. 1, 96-103.
10. Bruce, H. M. 1963 Olfactory block to pregnancy among grouped mice. J. Reprod. Fertil. 6, 451-460.
11. Chipman, R. K. & Fox, K. A. 1966 Oestrus synchronization and pregnancy blocking in wild house mice (Mus musculus). J. Reprod. Fertil. 12, 233-236.
12. Coopersmith, C. B. & Lenington, S. 1998 Pregnancy block in house mice (Mus domesticus) as a function of t-complex genotype: examination of the mate choice and male infanticide hypotheses. J. Comp. Psychol. 112, 82-91.
13. Dawkins, R. 1976 The selfish gene. Oxford, UK: Oxford University Press.
14. Desjardins, C., Maruniak, J. A. & Bronson, F. H. 1973 Social rank in house mice - differentiation revealed by ultraviolet visualization of urinary marking patterns. Science 182, 939-941.
15. deCatanzaro, D. & Murji, T. 2004 Inseminated female mice (Mus musculus) investigate rather than avoid novel males that disrupt pregnancy, but sires protect pregnancy. J. Comp. Psychol. 118, 251-257.
16. de la Maza, H. M., Wolff, J. O. & Lindsey, A. 1999 Exposure to strange adults does not cause pregnancy disruption or infanticide in the gray-tailed vole. Behav. Ecol. Sociobiol. 45, 107-113.
17. Drickamer, L. C. 1989 Pregnancy block in wild stock house mice, Mus domesticus - olfactory preferences of females during gestation. Anim. Behav. 37, 690-692.
18. Huck, U. W. 1982 Pregnancy block in laboratory mice as a function of male social status. J. Reprod. Fertil. 66, 181-184.
19. Hurst, J. L. 1987 Behavioral variation in wild house mice Mus domesticus rutty - a quantitative assessment of female social organization. Anim. Behav. 35, 1846-1857.
20. Kaba, H., Rosser, A. & Keverne, B. 1989 Neural basis of olfactory memory in the context of pregnancy block. Neuroscience 32, 657-662. (Pubitemid 20008294)
21. Keverne, E. B. & Brennan, P. A. 1996 Olfactory recognition memory. J. Physiol. (Paris) 90, 399-401.
22. Keverne, E. B. & de la Riva, C. 1982 Pheromones in mice: reciprocal interaction between the nose and brain. Nature 296, 148-150. (Pubitemid 12160908)
23. Kumar, A. & Dominic, C. J. 1993 Male-induced implantation failure (the Bruce effect) in mice: protective effect of familiar males on implantation. Physiol. Behav. 54, 1169-1172.
24. Labov, J. B. 1981a Male social status, physiology, and ability to block pregnancies in female house mice (Mus musculus). Behav. Ecol. Sociobiol. 8, 287-291.
25. Labov, J. B. 1981b Pregnancy blocking in rodents: adaptive advantages for females. Am. Nat. 118, 361-371.
26. Leinders-Zufall, T. et al. 2004 MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 306, 1033-1037. (Pubitemid 39482906)
27. Luo, M., Fee, M. S. & Katz, L. C. 2003 Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 299, 1196-1201. (Pubitemid 36237454)
28. Mahady, S. J. & Wolff, J. O. 2002 A field test of the Bruce effect in the monogamous prairie vole (Microtus ochrogaster). Behav. Ecol. Sociobiol. 52, 31-37.
29. Meredith, M. & O'Connell, R. J. 1979 Efferent control of stimulus access to the hamster vomeronasal organ. J. Physiol. 286, 301-316. (Pubitemid 9085485)
30. Michael, S. D. 1976 Plasma prolactin and progesterone during the oestrus cycle in the mouse. Proc. Soc. Exp. Biol. Med. 153, 254-257.
31. Nagasawa, H., Miyamoto, M. & Fujimoto, M. 1973 Reproductivity in inbred strains of mice and project for their efficient production. Exp. Anim. 22, 119-126.
32. Parkes, A. S. & Bruce, H. M. 1961 Olfactory stimuli in mammalian reproduction. Science 134, 1049-1054.
33. Peele, P., Salazar, I., Mimmack, M., Keverne, E. B. & Brennan, P. A. 2003 Low molecular weight constituents of male mouse urine mediate the pregnancy block effect and convey information about the identity of the mating male. Eur. J. Neurosci. 18, 622-628.
34. Peripato, A. C., de Brito, R. A., Vaughn, T. T., Pletscher, L. S., Matioli, S. R. & Cheverud, J. M. 2002 Quantitative trait loci for maternal performance for offspring survival in mice. Genetics 162, 1341-1353. (Pubitemid 35417524)
35. Rajendren, G. & Dominic, C. J. 1993 The male-induced implantation failure (the Bruce effect) in mice: effect of exogenous progesterone on maintenance of pregnancy in male-exposed females. Exp. Clin. Endocrinol. 101, 356-359.
36. Refinetti, R. 2004 Daily activity patterns of a nocturnal and a diurnal rodent in a seminatural environment. Physiol. Behav. 82, 285-294.
37. Rosser, A. E. & Keverne, E. B. 1985 The importance of central noradrenergic neurons in the formation of an olfactory memory in the prevention of pregnancy block. Neuroscience 15, 1141-1147. (Pubitemid 15226672)
38. Rosser, A. E., Remfry, C. J. & Keverne, E. B. 1989 Restricted exposure of mice to primer pheromones coincident with prolactin surges blocks pregnancy by changing hypothalamic dopamine release. J. Reprod. Fertil. 87, 553-559.
39. Ryan, K. D. & Schwartz, N. B. 1980 Changes in serum hormone levels associated with male-induced ovulation in group-housed adult female mice. Endocrinology 106, 959-966. (Pubitemid 10135135)
40. Rülicke, T., Guncz, N. & Wedekind, C. 2006 Early maternal investment in mice: no evidence for compatible-genes sexual selection despite hybrid vigor. J. Evol. Biol. 19, 922-928.
41. Schradin, C. 2008 Differences in prolactin levels between three alternative male reproductive tactics in striped mice (Rhabdomys pumilio). Proc. R. Soc. B 275, 1047-1052.
42. Schwagmeyer, P. L. 1979 Bruce effect-evaluation of male-female advantages. Am. Nat. 114, 932-938.
43. Southwick, C. H. 1955 Regulatory mechanisms of house mouse populations: social behavior affecting litter survival. Ecology 36, 627-634.
44. Stehn, R. A. & Jannett, F. J. 1981 Male-induced abortion in various microtine rodents. J. Mammal. 62, 369-372.
45. Storey, A. E. 1986 Influence of sires on male-induced pregnancy disruptions in meadow voles (Microtus pennsylvanicus) differs with stage of pregnancy. J. Comp. Psychol. 100, 15-20.
46. Storey, A. E., Delahunty, K. M., McKay, D. W., Walsh, C. J. & Wilhelm, S. I. 2006 Social and hormonal bases of individual differences in the parental behaviour of birds and mammals. Can. J. Exp. Psychol. 60, 237-245.
47. Stormshak, F., Zelinski-Wooten, M. B. & Abdelgadir, S. E. 1987 Comparative aspects of the regulation of corpus luteum function in various species. Adv. Exp. Med. Biol. 219, 327-360.
48. Torner, L., Toschi, N., Pohlinger, A., Landgraf, R. & Neumann, I. D. 2001 Anxiolytic and anti-stress effects of brain prolactin: improved efficacy of antisense targeting of the prolactin receptor by molecular modeling. J. Neurosci. 21, 3207-3214. (Pubitemid 32323502)
49. Vom Saal, F. S., Franks, P., Boechler, M., Palanza, P. & Parmigiani, S. 1995 Nest defence and survival of offspring in highly aggressive wild canadian female house mice. Physiol. Behav. 58, 669-678.
50. Wolff, R. J. 1985 Mating behaviour and female choice: their relation to social structure in wild caught house mice (Mus musculus) housed in a semi-natural environment. J. Zool. 207, 43-51.
51. Yamazaki, K., Beauchamp, G. K. & Wysocki, C. J. 1983 Recognition of H-2 types in relation to the blocking of pregnancy in mice. Science 221, 186-188.