Bruce effect
Encyclopedia
The Bruce effect, or pregnancy block, refers to the tendency for female
rodent
s to terminate their pregnancies
following exposure to the scent of an unfamiliar male
. The effect has primarily been studied in laboratory mice (Mus musculus), but is also observed in deer-mice, meadow vole
s, and collared lemming
s. The Bruce Effect has also been proposed, but not confirmed, in non-rodent species such as the lion
. In mice, pregnancy can only be terminated prior to embryo implantation, but other species will interrupt even a late-term pregnancy. The Bruce Effect was first noted in 1959 by Hilda M. Bruce
.
housed pregnant mice with male mice that were not the father of the carried embryo
. As a result, the rate of miscarriage
s 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.
contains MHC class I
peptides that bind to receptors in the female’s vomeronasal organ
, a mucus-filled
structure in the nasal septum
. These chemical signals, which are specific to each male, are learnt by the female during mating, or shortly after. 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.
to these pheromones. The pregnancy disruption will, thus, be averted. This role for noradrenaline has recently been called into question. 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.
, and stria terminalis. These areas stimulate the hypothalamus
to increase the release of dopamine
, which thus prevents the secretion of prolactin from the anterior pituitary. In the absence of prolactin
, an essential hormone for maintaining the corpus luteum
, luteolysis
takes place. As the corpus luteum can no longer release progesterone
, the uterus
remains unprimed for embryo implantation, and the pregnancy fails.
such as E2 can enter the bloodstream directly via nasal
ingestion
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. Castrated males are incapable of terminating female pregnancies, except when castrated males are given testosterone
. Oestradiol, a metabolic product of testosterone, is known to disrupt pregnancy in females, and is present in male urine.
. Pregnancy is only terminated if exposure to novel male scent coincides with two prolactin surges, one of these occurring in a daylight period
.
and persisted in the population, the Bruce Effect must afford individuals a fitness advantage
. The possible advantages of pregnancy block are widely debated.
, reserving their reproductive resources for the highest-quality male. Certainly, females are more likely to seek proximity to dominant males. 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. The Bruce Effect is most common in polygynous rodent species, for which the risk of infanticide is highest.
Female
Female is the sex of an organism, or a part of an organism, which produces non-mobile ova .- Defining characteristics :The ova are defined as the larger gametes in a heterogamous reproduction system, while the smaller, usually motile gamete, the spermatozoon, is produced by the male...
rodent
Rodent
Rodentia is an order of mammals also known as rodents, characterised by two continuously growing incisors in the upper and lower jaws which must be kept short by gnawing....
s to terminate their pregnancies
Pregnancy
Pregnancy refers to the fertilization and development of one or more offspring, known as a fetus or embryo, in a woman's uterus. In a pregnancy, there can be multiple gestations, as in the case of twins or triplets...
following exposure to the scent of an unfamiliar male
Male
Male refers to the biological sex of an organism, or part of an organism, which produces small mobile gametes, called spermatozoa. Each spermatozoon can fuse with a larger female gamete or ovum, in the process of fertilization...
. The effect has primarily been studied in laboratory mice (Mus musculus), but is also observed in deer-mice, meadow vole
Meadow Vole
The Meadow Vole , sometimes called the Field Mouse or Meadow Mouse, is a North American vole found across Canada, Alaska and the northern United States. Its range extends further south along the Atlantic coast. One subspecies, the Florida Salt Marsh Vole , is found in Florida, and is classified as...
s, and collared lemming
Collared lemming
Dicrostonyx is a genus of rodent in the family Cricetidae. It contains the collared lemmings.It contains the following species:* Northern Collared Lemming * Ungava Collared Lemming...
s. The Bruce Effect has also been proposed, but not confirmed, in non-rodent species such as the lion
Lion
The lion is one of the four big cats in the genus Panthera, and a member of the family Felidae. With some males exceeding 250 kg in weight, it is the second-largest living cat after the tiger...
. In mice, pregnancy can only be terminated prior to embryo implantation, but other species will interrupt even a late-term pregnancy. The Bruce Effect was first noted in 1959 by Hilda M. Bruce
Hilda Bruce
Hilda Margaret Bruce was a British zoologist, best known for her discovery of the Bruce effect, a pheromonal behaviour observed in many rodent species.-Biography:...
.
Discovery
In an experiment published in 1959, zoologist Hilda BruceHilda Bruce
Hilda Margaret Bruce was a British zoologist, best known for her discovery of the Bruce effect, a pheromonal behaviour observed in many rodent species.-Biography:...
housed pregnant mice with male mice that were not the father of the carried embryo
Embryo
An embryo is a multicellular diploid eukaryote in its earliest stage of development, from the time of first cell division until birth, hatching, or germination...
. As a result, the rate of miscarriage
Miscarriage
Miscarriage or spontaneous abortion is the spontaneous end of a pregnancy at a stage where the embryo or fetus is incapable of surviving independently, generally defined in humans at prior to 20 weeks of gestation...
s 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.
Detection of pheromones
The vomeronasal system serves as a “vascular pump” that, stimulated by the presence of a novel male, actively draws in substances. Male mouse urineUrine
Urine is a typically sterile liquid by-product of the body that is secreted by the kidneys through a process called urination and excreted through the urethra. Cellular metabolism generates numerous by-products, many rich in nitrogen, that require elimination from the bloodstream...
contains MHC class I
MHC class I
MHC class I molecules are one of two primary classes of major histocompatibility complex molecules and are found on every nucleated cell of the body...
peptides that bind to receptors in the female’s vomeronasal organ
Vomeronasal organ
The vomeronasal organ , or Jacobson's organ, is an auxiliary olfactory sense organ that is found in many animals. It was discovered by Frederik Ruysch and later by Ludwig Jacobson in 1813....
, a mucus-filled
Mucus
In vertebrates, mucus is a slippery secretion produced by, and covering, mucous membranes. Mucous fluid is typically produced from mucous cells found in mucous glands. Mucous cells secrete products that are rich in glycoproteins and water. Mucous fluid may also originate from mixed glands, which...
structure in the nasal septum
Nasal septum
The nasal septum separates the left and right airways in the nose, dividing the two nostrils.It is depressed by the Depressor septi nasi muscle.-Composition:The fleshy external end of the nasal septum is sometimes also called columella....
. These chemical signals, which are specific to each male, are learnt by the female during mating, or shortly after. The hormone vasopressin
Vasopressin
Arginine vasopressin , also known as vasopressin, argipressin or antidiuretic hormone , is a neurohypophysial hormone found in most mammals, including humans. Vasopressin is a peptide hormone that controls the reabsorption of molecules in the tubules of the kidneys by affecting the tissue's...
is crucial in coupling a chemosensory cue with an appropriate physiological response. When the vasopressin 1b receptor
Arginine vasopressin receptor 1B
Arginine vasopressin receptor 1B is a protein that acts as receptor for arginine vasopressin. AVPR1B belongs to the subfamily of G-protein coupled receptors...
gene is knocked out in females, the presence of an unfamiliar male does not trigger pregnancy disruption.
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 bulbOlfactory bulb
The olfactory bulb is a structure of the vertebrate forebrain involved in olfaction, the perception of odors.-Anatomy:In most vertebrates, the olfactory bulb is the most rostral part of the brain. In humans, however, the olfactory bulb is on the inferior side of the brain...
to these pheromones. The pregnancy disruption will, thus, be averted. This role for noradrenaline has recently been called into question. The hormone oxytocin
Oxytocin
Oxytocin is a mammalian hormone that acts primarily as a neuromodulator in the brain.Oxytocin is best known for its roles in sexual reproduction, in particular during and after childbirth...
is also important in this social memory
Memory
In psychology, memory is an organism's ability to store, retain, and recall information and experiences. Traditional studies of memory began in the fields of philosophy, including techniques of artificially enhancing memory....
process. Females treated with an oxytocin antagonist
Antagonist
An antagonist is a character, group of characters, or institution, that represents the opposition against which the protagonist must contend...
are unable to recognise the urinary scent of their mate, and will terminate pregnancy when exposed to any male, known or unknown.
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 tractOlfactory tract
The olfactory tract is a bundle of axons connecting the mitral and tufted cells of the olfactory bulb to several target regions in the brain, including piriform cortex, amygdala, and entorhinal cortex...
, and stria terminalis. These areas stimulate the hypothalamus
Hypothalamus
The Hypothalamus is a portion of the brain that contains a number of small nuclei with a variety of functions...
to increase the release of dopamine
Dopamine
Dopamine is a catecholamine neurotransmitter present in a wide variety of animals, including both vertebrates and invertebrates. In the brain, this substituted phenethylamine functions as a neurotransmitter, activating the five known types of dopamine receptors—D1, D2, D3, D4, and D5—and their...
, which thus prevents the secretion of prolactin from the anterior pituitary. In the absence of prolactin
Prolactin
Prolactin also known as luteotropic hormone is a protein that in humans is encoded by the PRL gene.Prolactin is a peptide hormone discovered by Henry Friesen...
, an essential hormone for maintaining the corpus luteum
Corpus luteum
The corpus luteum is a temporary endocrine structure in mammals, involved in production of relatively high levels of progesterone and moderate levels of estradiol and inhibin A...
, luteolysis
Luteolysis
Luteolysis is the structural and functional degradation of the corpus luteum , which occurs at the end of the luteal phase of both the estrous and menstrual cycles in the absence of pregnancy. In domestic animals, luteolysis is inititated by the hormones prostaglandin F2alpha and oxytocin...
takes place. As the corpus luteum can no longer release progesterone
Progesterone
Progesterone also known as P4 is a C-21 steroid hormone involved in the female menstrual cycle, pregnancy and embryogenesis of humans and other species...
, the uterus
Uterus
The uterus or womb is a major female hormone-responsive reproductive sex organ of most mammals including humans. One end, the cervix, opens into the vagina, while the other is connected to one or both fallopian tubes, depending on the species...
remains unprimed for embryo implantation, and the pregnancy fails.
Role of oestrogens
Androgens and oestrogens, particularly oestradiol (E2), are also crucial chemosignals regulating the Bruce Effect. However, they are believed to act via a separate pathway to that discussed above. Small steroid moleculesSteroid hormone
A steroid hormone is a steroid that acts as a hormone. Steroid hormones can be grouped into five groups by the receptors to which they bind: glucocorticoids, mineralocorticoids, androgens, estrogens, and progestogens...
such as E2 can enter the bloodstream directly via nasal
Nose
Anatomically, a nose is a protuberance in vertebrates that houses the nostrils, or nares, which admit and expel air for respiration in conjunction with the mouth. Behind the nose are the olfactory mucosa and the sinuses. Behind the nasal cavity, air next passes through the pharynx, shared with the...
ingestion
Ingestion
Ingestion is the consumption of a substance by an organism. In animals, it normally is accomplished by taking in the substance through the mouth into the gastrointestinal tract, such as through eating or drinking...
and travel to the uterus
Uterus
The uterus or womb is a major female hormone-responsive reproductive sex organ of most mammals including humans. One end, the cervix, opens into the vagina, while the other is connected to one or both fallopian tubes, depending on the species...
, which has a high density of suitable receptors. Normally, E2 is essential in preparing both the blastocyst
Blastocyst
The blastocyst is a structure formed in the early embryogenesis of mammals, after the formation of the morula. It is a specifically mammalian example of a blastula. It possesses an inner cell mass , or embryoblast, which subsequently forms the embryo, and an outer layer of cells, or trophoblast,...
and uterus
Uterus
The uterus or womb is a major female hormone-responsive reproductive sex organ of most mammals including humans. One end, the cervix, opens into the vagina, while the other is connected to one or both fallopian tubes, depending on the species...
for implantation. However, excessive E2 will prevent implantation from taking place. Castrated males are incapable of terminating female pregnancies, except when castrated males are given testosterone
Testosterone
Testosterone is a steroid hormone from the androgen group and is found in mammals, reptiles, birds, and other vertebrates. In mammals, testosterone is primarily secreted in the testes of males and the ovaries of females, although small amounts are also secreted by the adrenal glands...
. Oestradiol, a metabolic product of testosterone, is known to disrupt pregnancy in females, 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 prolactinProlactin
Prolactin also known as luteotropic hormone is a protein that in humans is encoded by the PRL gene.Prolactin is a peptide hormone discovered by Henry Friesen...
. Pregnancy is only terminated if exposure to novel male scent coincides with two prolactin surges, one of these occurring in a daylight period
Photoperiodism
Photoperiodism is the physiological reaction of organisms to the length of day or night. It occurs in plants and animals.Photoperiodism can also be defined as the developmental responses of plants to the relative lengths of the light and dark periods...
.
Evolutionary benefits
In order to have evolvedEvolution
Evolution is any change across successive generations in the heritable characteristics of biological populations. Evolutionary processes give rise to diversity at every level of biological organisation, including species, individual organisms and molecules such as DNA and proteins.Life on Earth...
and persisted in the population, the Bruce Effect must afford individuals a fitness advantage
Fitness (biology)
Fitness is a central idea in evolutionary theory. It can be defined either with respect to a genotype or to a phenotype in a given environment...
. 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. This allows males to improve their fitness success by “sabotaging” the pregnancy of a male competitor, and more quickly returning the female to oestrus. The Bruce Effect can also aid in maintaining social status, with dominant males leaving more urinal scent markings, 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. In this way, females can exert a post-copulatory mate choiceMate choice
Mate choice, or intersexual selection, is an evolutionary process in which selection of a mate depends on attractiveness of its traits. It is one of two components of sexual selection...
, reserving their reproductive resources for the highest-quality male. Certainly, females are more likely to seek proximity to dominant males. In many rodent species, males perform infanticide
Infanticide
Infanticide or infant homicide is the killing of a human infant. Neonaticide, a killing within 24 hours of a baby's birth, is most commonly done by the mother.In many past societies, certain forms of infanticide were considered permissible...
on unrelated young; pregnancy block may avoid the wasted investment of gestating offspring likely to be killed at birth. The Bruce Effect is most common in polygynous rodent species, for which the risk of infanticide is highest.
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