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The Bruce effect, or pregnancy block,[1][2] refers to the tendency for female rodents to terminate their pregnancies following exposure to the scent of an unfamiliar male.[3] The effect has primarily been studied in laboratory mice (Mus musculus),[1] but is also observed in deer-mice,[4] meadow voles,[5] and collared lemmings.[6] The Bruce Effect has also been proposed, but not confirmed, in non-rodent species such as the lion.[7] In mice, pregnancy can only be terminated prior to embryo implantation, but other species will interrupt even a late-term pregnancy.[8] The Bruce Effect was first noted in 1959 by Hilda M. Bruce.[9]

Discovery

In an experiment published in 1959, zoologist Hilda Bruce housed pregnant mice with male mice that were not the father of the carried embryo. As a result, the rate of miscarriages increased, followed by mating with the new male. No increased rate of miscarriages occurred when pregnant mice were paired with castrated or juvenile male mice.

Mechanisms of action

Detection of pheromones

The vomeronasal system serves as a “vascular pump” that, stimulated by the presence of a novel male, actively draws in substances.[10] Male mouse urine contains MHC class I peptides that bind to receptors in the female’s vomeronasal organ,[3][11] a mucus-filled structure in the nasal septum.[12] These chemical signals, which are specific to each male, are learnt by the female during mating,[13] or shortly after.[3] The hormone vasopressin is crucial in coupling a chemosensory cue with an appropriate physiological response. When the vasopressin 1b receptor gene is knocked out in females, the presence of an unfamiliar male does not trigger pregnancy disruption.[14]

Recognising familiar males

Exposure to a male’s urinal pheromones will activate a neuroendocrine pathway leading to pregnancy failure. However, if the pheromones correspond with those memorised by the female (usually the male mating partner), a release of noradrenaline will lower the receptivity of the accessory olfactory bulb to these pheromones.[13] The pregnancy disruption will, thus, be averted. This role for noradrenaline has recently been called into question.[12] The hormone oxytocin is also important in this social memory process. Females treated with an oxytocin antagonist are unable to recognise the urinary scent of their mate, and will terminate pregnancy when exposed to any male, known or unknown.[15]

Neuroendocrine pathway

The activation of vomeronasal neuron receptors by male pheromones triggers a complex neuroendocrine pathway. The pheromonal information travels via nerves to the accessory olfactory bulb, and then to the corticomedial amygdala, accessory olfactory tract, and stria terminalis.[12] These areas stimulate the hypothalamus to increase the release of dopamine,[12][16] which thus prevents the secretion of prolactin from the anterior pituitary.[3] In the absence of prolactin, an essential hormone for maintaining the corpus luteum, luteolysis takes place.[3] As the corpus luteum can no longer release progesterone, the uterus remains unprimed for embryo implantation, and the pregnancy fails.[16]

Role of oestrogens

Androgens and oestrogens, particularly oestradiol (E2), are also crucial chemosignals regulating the Bruce Effect.[10] However, they are believed to act via a separate pathway to that discussed above. Small steroid molecules such as E2 can enter the bloodstream directly via nasal ingestion[10] and travel to the uterus, which has a high density of suitable receptors. Normally, E2 is essential in preparing both the blastocyst and uterus for implantation. However, excessive E2 will prevent implantation from taking place.[17][18] Castrated males are incapable of terminating female pregnancies,[19] except when castrated males are given testosterone.[10] Oestradiol, a metabolic product of testosterone, is known to disrupt pregnancy in females,[10] and is present in male urine.

Timing

The incidence of the Bruce Effect depends on the timing of pheromone exposure. Post-mating, females experience twice-daily surges of prolactin.[3] Pregnancy is only terminated if exposure to novel male scent coincides with two prolactin surges, one of these occurring in a daylight period.[16]

Evolutionary benefits

In order to have evolved and persisted in the population, the Bruce Effect must afford individuals a fitness advantage.[3] The possible advantages of pregnancy block are widely debated.

Males

When given the opportunity, male mice tend to direct their urine in the female’s direction.[20] This allows males to improve their fitness success by “sabotaging” the pregnancy of a male competitor,[3] and more quickly returning the female to oestrus.[21] The Bruce Effect can also aid in maintaining social status, with dominant males leaving more urinal scent markings,[22] and so blocking the pregnancies of subordinate males.

Females

Females can control their likelihood of terminating pregnancy by pursuing or avoiding novel male contact during their most susceptible periods.[23] In this way, females can exert a post-copulatory mate choice, reserving their reproductive resources for the highest-quality male. Certainly, females are more likely to seek proximity to dominant males.[23] In many rodent species, males perform infanticide on unrelated young; pregnancy block may avoid the wasted investment of gestating offspring likely to be killed at birth.[8][24] The Bruce Effect is most common in polygynous rodent species, for which the risk of infanticide is highest.[25]

See also

References

  1. 1.0 1.1 Heske E.J. and Nelson R.J. (1984) “Pregnancy Interruption in Microtus ochrogaster: Laboratory Artifact or Field Phenomenon?” Biology of Reproduction, 31: 97-103
  2. Hofmann J.E., Getz L.L, and Gavish L. (1987) “Effect of Multiple Short-Term Exposures of Pregnant Microtus ochrogaster to Strange Males,” Journal of Mammalogy, 68(1): 166-169
  3. 3.0 3.1 3.2 3.3 3.4 3.5 3.6 3.7 Becker S.D. and Hurst J.L. (2007) “Pregnancy from a Female Perspective,” Chemical Signals in Vertebrates, 11(3): 141-150
  4. Eleftheriou B.E., Bronson F.H., and Zarrow M.X. (1962) “Interaction of Olfactory and Other Environmental Stimuli on Implantation in the Deer Mouse,” Science, 137(3532): 764
  5. Clulow F.V. and Langford P.E. (1971) “Pregnancy-block in the meadow vole, Microtus pennsylvanicus,” Journal of Reproduction and Fertility, 24: 275-277
  6. Mallory F.F. and Brooks R.J. (1980) “Infanticide and Pregnancy Failure: Reproductive Strategies in the Female Collared Lemming (Dicrostonyx groenlandicus),” Biology of Reproduction, 22:192-196.
  7. Packer C. and Pusey A.E. (1983) “Adaptations of female lions to infanticide by incoming males,” The American Naturalist, 121(5): 716-728
  8. 8.0 8.1 Labov J.B. (1981) “Pregnancy Blocking in Rodents: Adaptive Advantages for Females,” The American Naturalist, 118(3): 361-371
  9. Bruce H.M. (1959) “An exteroceptive block to pregnancy in the mouse” Nature, 184:105
  10. 10.0 10.1 10.2 10.3 10.4 Guzzo A.C., Berger R.G., and deCatanzaro D. (2010) “Excretion and binding of tritium-labelled oestradiol in mice (Mus musculus): implications for the Bruce effect,” Reproduction, 139: 255-263
  11. Zufall F. and Leinders-Zufall T. (2007) “Mammalian pheromone sensing,” Current Opinion in Neurobiology, 17:483-489
  12. 12.0 12.1 12.2 12.3 Brennan P.A. (2009) “Outstanding issues surrounding vomeronasal mechanisms of pregnancy block and individual recognition in mice,” Behavioural Brain Research, 200: 287-294
  13. 13.0 13.1 Brennan P.A. and Zufall F. (2006) “Pheromonal communication in vertebrates,” Nature, 444: 308-315
  14. Wersinger S.R., Temple J.L., Caldwell H.K., Young W.S. (2008) “Inactivation of the Oxytocin and the Vasopressin (Avp) 1b Receptor Genes, But Not the Avp 1a Receptor Gene, Differentially Impairs the Bruce Effect in Laboratory Mice (Mus musculus),” Endocrinology, 149: 116-121
  15. Neumann I.D. (2008) “Brain Oxytocin: A Key Regulator of Emotional and Social Behaviours in Both Females and Males,” Journal of Neuroendocrinology, 20:858-865
  16. 16.0 16.1 16.2 Rosser A.E., Remfry C.J., and Keverne E.B. (1989) “Restricted exposure of mice to primer pheromones coincident with prolactin surges blocks pregnancy by changing hypothalamic dopamine release,” Journal of Reproduction and Fertility, 87: 553-559
  17. Valbuena D., Martin J., de Pablo J.L., Remohí J., Pellicer A., and Simón C. (2001) “Increasing levels of estradiol are deleterious to embryonic implantation because they directly affect the embryo,” Fertility and Sterility, 76(5): 962-968
  18. Ma W., Song H., Das S.K., Paria B.C., and Dey S.K. (2003) “Estrogen is a critical determinant that specifies the duration of the window of uterine receptivity for implantation,” Proceedings of the National Academy of Sciences of the United States of America, 100(5): 2963-2968
  19. Bruce H.M. (1965) “Effect of castration on the reproductive pheromones of male mice,” Journal of Reproduction and Fertility, 10: 141-143
  20. deCatanzaro D., Khan A., Berger R.G., and Lewis E. (2009) “Exposure to developing females induces polyuria, polydipsia, and altered urinary levels of creatinine, 17β-estradiol, and testosterone in adult male mice (Mus musculus),” Hormones and Behavior, 55: 240-247
  21. Huck U.W. (1982) “Pregnancy block in laboratory mice as a function of male social status,” Journal of Reproduction and Fertility, 66: 181-184
  22. Desjardins C., Maruniak J.A., and Bronson F.H. (1973) “Social Rank in House Mice: Differentiation Revealed by Ultraviolet Visualization of Urinary Marking Patterns,” Science, 182(4115): 939-941
  23. 23.0 23.1 Becker S.D. and Hurst J.L. (2009) “Female behaviour plays a critical role in controlling murine pregnancy block,” Proceedings of the Royal Society B, 276: 1723-1729.
  24. Schwagmeyer P.L. (1979) “The Bruce Effect: an evaluation of male/female advantages,” The American Naturalist, 114(6): 932-938
  25. Pillay N. and Kinahan A.A. (2009) “Mating strategy predicts the occurrence of the Bruce effect in the vlei rat Otomys irroratus,” Behaviour, 146: 139-151

Further reading

  • de la Maza HM, Wolff JO, Lindsey A (1999) "Exposure to strange males does not cause pregnancy disruption or infanticide in the gray-tailed vole," Behavioral Ecology and Sociobiology, 45: 107–113
  • Kenney AM, Evans RL, Dewsbury DA. (1977) "Postimplantation pregnancy disruption in Microtus ochrogaster, Microtus pennsylvanicus, and Peromyscus maniculatus," Journal of Reproduction and Fertility, 49: 365–367
  • Mahady S, Wolff JO (2002) "A field test of the Bruce effect in the monogamous prairie vole, Microtus ochrogaster," Behavioral Ecology and Sociobiology, 52: 31–37.
  • Stehn RA, Richmond ME (1975) "Male-induced pregnancy termination in the prairie vole, Microtus ochrogaster," Science, 187: 1211–1213
  • Stehn RA, Jannett FJ Jr. (1981) "Male-induced abortion in various microtine rodents," Journal of Mammalogy, 62: 369–372
  • Storey AE, Snow DT (1990) "Postimplantation pregnancy disruptions in meadow voles: Relationship to variation in male sexual and aggressive behavior," Physiology and Behaviour, 47: 19–25
  • Storey AE. (1994) "Pre-implantation pregnancy disruptions in female meadow voles Microtus pennsylvanicus (Rodentia:Muridae): Male competition or female mate choice?" Ethology, 98: 89–100
  • Wolff, J. O. (2003) "Laboratory Studies with Rodents: Facts or Artifacts?" BioScience, 53:421-427


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