Infanticide in rodents

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California ground squirrel, one species known to show infanticide behaviour Cgs face.JPG
California ground squirrel, one species known to show infanticide behaviour

Infanticide is the termination of a neonate after it has been born, and in zoology this is often the termination or consumption of newborn animals by either a parent or an unrelated adult. In rodents, it is not uncommon for the mother to commit infanticide shortly after parturition (giving birth) under conditions of extreme stress (parental infanticide), or for an unrelated male to kill neonates (nonparental infanticide).

Contents

Parental infanticide

Parental infanticide is perhaps the most confusing behaviour to understand, as in many cases it can seem maladaptive for a parent to terminate offspring carrying its own genetic material. However, studies in mice have indicated infanticide may be a genetically heritable trait, [1] and may even have a learned element, [2] so there is clearly more to the behaviour than might be expected. The occurrence of infanticide seems to vary within rodent species between parents. For example, male meadow voles and house mice can be classed as either 'infanticidal' or 'non-infanticidal' depending on their history with other litters they have sired, although studies have shown that females do not discriminate between these classes when choosing a mate. [3] Furthermore, recent studies in rodents have shown that infanticide is influenced by various hormones such as: prolactin, corticosterone, and progesterone.

Evidence from studies on female cooperative breeding Mongolian gerbils indicated that type of living environment influences hormone concentrations of progesterone and prolactin. To investigate living environment effects, female gerbils in three housing groups (FH-family housed, PH-pair mate housed, and SH- singly housed) were observed and compared to each other. Unfamiliar pups were placed in a cage with each female to observe any infanticide response. Following the pup test samples of prolactin and progesterone were taken via blood. Analyses showed that females with lower progesterone (FH group) and prolactin levels rarely displayed infanticidal behavior toward the unfamiliar pup, compared to the females that possessed higher levels, in which they attacked the pup. These results show that cohabitation with family, contributes to lower progesterone and prolactin concentrations in female Mongolian gerbils, which is shown to decrease the likelihood that infanticide will occur. [4]

A further study investigated the role of living environment with younger siblings on infanticide in female and male cooperative breeding Mongolian gerbils. Female and male gerbils were put into one of four housing conditions (parents only, parents and siblings, siblings, and unrelated). Again, a pup test was conducted (same as previous study above), with each male and female to observe responses to an unfamiliar pup in the cage, while progesterone was measured via blood sample following the test. Females portrayed attacking behavior toward the unfamiliar pup when progesterone concentrations were elevated compared to the females with low concentrations (parents and siblings). Thus, these results have demonstrated further support that living with parents and siblings contributes strongly to lower levels of progesterone, causing inhibition of infanticide in female Mongolian gerbils. [5]

Researchers have found evidence on maternal care and infanticide in female mice that were pregnant or lactating, when placed in a dangerous or safe environment. Female mice were placed in soiled bedding, with unfamiliar fecal cues of males which modeled a dangerous environment (UMB), or they were placed in a safe environment (NB) with neutral bedding. Corticosterone levels were measured via fecal metabolites after exposure to the assigned bedding. Female mice in the dangerous living environment group, showed higher levels of fecal corticosterone, and minimal maternal care compared to the females in the safe environment group. Furthermore, a dangerous environment inherently provides infanticide threats to female mice, increasing the likelihood that corticosterone concentrations will increase, while maternal care toward offspring decreases. [6]

In a study on mated male mice, there is evidence shown that when progesterone receptors are tampered with, using an antagonist, infanticide behavior is declined, while caregiving is increased. Males were observed with their mate to evaluate parental behavior, and then were administered implants by capsules filled with sesame oil, or progesterone plus sesame oil, along with RU486 pellets as the antagonist. Aggressive behavior was measured by response toward litters, and progesterone was measured by blood samples. Results indicated that PRKO mice (the knock-out mice) did not commit infanticide, but showed more paternal behavior, in comparison to the C57BL/6 strain mice that committed infanticide. Thus, this indicates that aggression and paternal behavior in mated male mice is linked to progesterone receptors; that is, when progesterone receptors are blocked by RU486 antagonist, males are less aggressive, and more paternal toward offspring. [7]

Nonparental infanticide

Some rodent species (most typically males) will take the chance to kill neonates that are unrelated to them should opportunity permit. There is thought to be several benefits by doing so, which not only include nutrition benefits (particularly where food is in short supply [8] ) but also non-direct benefits, such as allowing access to more resources, improving reproductive opportunities and the retainment of energy and resources that might otherwise be spent on unrelated offspring. [9] A common causal factor of infanticide, particularly among sciurid rodents, is direct resource competition, therefore killing the pups of an unrelated neighbour would prevent resource competition with those individuals in the future. [10]

Species known to commit infanticide

Work by Blumstein (2000) [11] highlighted the following rodent species which have previously been associated with infanticide in published scientific literature. Assessment of these traits lead Blumstein to conclude that infanticide evolved independently in sciuromorphs, myomorphs and caviomorphs.

Exceptions

Common degus do not show this behaviour. Octodon degus BG.jpg
Common degus do not show this behaviour.

Not all rodent species commit infanticide, and in fact some species are remarkable for their lack of this behaviour. One such species is the common degu, a highly social caviomorph rodent from central Chile. Common degus have been found not to harm even unfamiliar pups, and male degus will even accept other males' litters into a group without problems. [12] This is thought to be related to the communal nesting habits of the species [13] and reflects genetic trends rather than a lack of the conditions that lead to infanticide.

Related Research Articles

<span class="mw-page-title-main">Prolactin</span> Protein family and hormone

Prolactin (PRL), also known as lactotropin, is a protein best known for its role in enabling mammals to produce milk. It is influential in over 300 separate processes in various vertebrates, including humans. Prolactin is secreted from the pituitary gland in response to eating, mating, estrogen treatment, ovulation and nursing. It is secreted heavily in pulses in between these events. Prolactin plays an essential role in metabolism, regulation of the immune system and pancreatic development.

<span class="mw-page-title-main">Common degu</span> Species of rodent (Octodon degus)

The common degu, or, historically, the degu, is a small hystricomorpha rodent endemic to the Chilean matorral ecoregion of central Chile. The name degu on its own indicates either the entire genus Octodon or, more commonly, just the common degu. Common degus belong to the parvorder Caviomorpha of the infraorder Hystricognathi, along with the chinchilla and guinea pig. The word degu comes from the indigenous language of Chile, Mapudungun, and the word dewü, meaning 'mouse' or 'rat'.

<span class="mw-page-title-main">Mongolian gerbil</span> Species of mammal

The Mongolian gerbil or Mongolian jird is a small rodent belonging to the subfamily Gerbillinae. Their body size is typically 110–135 mm, with a 95–120 mm tail, and body weight 60–130 g, with adult males larger than females. The animal is used in science and kept as a small house pet. Their use in science dates back to the latter half of the 19th century, but they only started to be kept as pets in the English-speaking world after 1954, when they were brought to the United States. However, their use in scientific research has fallen out of favor.

In mammalian species, pseudopregnancy is a physical state whereby all the signs and symptoms of pregnancy are exhibited, with the exception of the presence of a fetus, creating a false pregnancy. The corpus luteum is responsible for the development of maternal behavior and lactation, which are mediated by the continued production of progesterone by the corpus luteum through some or all of pregnancy. In most species, the corpus luteum is degraded in the absence of a pregnancy. However, in some species, the corpus luteum may persist in the absence of pregnancy and cause "pseudopregnancy", in which the female will exhibit clinical signs of pregnancy.

<span class="mw-page-title-main">Rodents as pets</span> Small pet mammal, possibly exotic

The most common rodents kept as household pets are hamsters, gerbils, common degus, fancy mice, fancy rats, common chinchillas, and guinea pigs (cavies).

<span class="mw-page-title-main">Alloparenting</span> Parenting not done by the birth parents

Alloparenting is a term used to classify any form of parental care provided by an individual towards young that are not its own direct offspring. These are often referred to as "non-descendant" young, even though grandchildren can be among them. Among humans, alloparenting is often performed by a child's grandparents and older siblings. Individuals providing this care are referred to using the neutral term of alloparent.

<span class="mw-page-title-main">Reproductive suppression</span>

Reproductive suppression is the prevention or inhibition of reproduction in otherwise healthy adult individuals. It includes delayed sexual maturation (puberty) or inhibition of sexual receptivity, facultatively increased interbirth interval through delayed or inhibited ovulation or spontaneous or induced abortion, abandonment of immature and dependent offspring, mate guarding, selective destruction and worker policing of eggs in some eusocial insects or cooperatively breeding birds, and infanticide, and infanticide in carnivores of the offspring of subordinate females either by directly killing by dominant females or males in mammals or indirectly through the withholding of assistance with infant care in marmosets and some carnivores. The Reproductive Suppression Model argues that "females can optimize their lifetime reproductive success by suppressing reproduction when future conditions for the survival of offspring are likely to be greatly improved over present ones”. When intragroup competition is high it may be beneficial to suppress the reproduction of others, and for subordinate females to suppress their own reproduction until a later time when social competition is reduced. This leads to reproductive skew within a social group, with some individuals having more offspring than others. The cost of reproductive suppression to the individual is lowest at the earliest stages of a reproductive event and reproductive suppression is often easiest to induce at the pre-ovulatory or earliest stages of pregnancy in mammals, and greatest after a birth. Therefore, neuroendocrine cues for assessing reproductive success should evolve to be reliable at early stages in the ovulatory cycle. Reproductive suppression occurs in its most extreme form in eusocial insects such as termites, hornets and bees and the mammalian naked mole rat which depend on a complex division of labor within the group for survival and in which specific genes, epigenetics and other factors are known to determine whether individuals will permanently be unable to breed or able to reach reproductive maturity under particular social conditions, and cooperatively breeding fish, birds and mammals in which a breeding pair depends on helpers whose reproduction is suppressed for the survival of their own offspring. In eusocial and cooperatively breeding animals most non-reproducing helpers engage in kin selection, enhancing their own inclusive fitness by ensuring the survival of offspring they are closely related to. Wolf packs suppress subordinate breeding.

<span class="mw-page-title-main">Estrogen insensitivity syndrome</span> Medical condition

Estrogen insensitivity syndrome (EIS), or estrogen resistance, is a form of congenital estrogen deficiency or hypoestrogenism which is caused by a defective estrogen receptor (ER) – specifically, the estrogen receptor alpha (ERα) – that results in an inability of estrogen to mediate its biological effects in the body. Congenital estrogen deficiency can alternatively be caused by a defect in aromatase, the enzyme responsible for the biosynthesis of estrogens, a condition which is referred to as aromatase deficiency and is similar in symptomatology to EIS.

<span class="mw-page-title-main">Infanticide (zoology)</span> Killing of young offspring by an adult animal of the same species

In animals, infanticide involves the intentional killing of young offspring by a mature animal of the same species. Animal infanticide is studied in zoology, specifically in the field of ethology. Ovicide is the analogous destruction of eggs. The practice has been observed in many species throughout the animal kingdom, especially primates but including microscopic rotifers, insects, fish, amphibians, birds and mammals. Infanticide can be practiced by both males and females.

<span class="mw-page-title-main">Nesting instinct</span> Instinct in pregnant animals related to estradiol

Nesting behavior refers to an instinct or urge in pregnant animals associated with an increase of estradiol (E2) to prepare a home for the upcoming newborn(s). Nest building provides protection against predators and competitors that mean to exploit or kill infants. It also aids in family structure and is therefore influenced by different mating behaviours and social settings. It is found in a variety of animals such as birds, fish, squirrels, mice and pigs, and is said to be done by humans as well. However, recent research into nesting tendencies in women has questioned whether there is really any biological basis for nesting in humans, positing a social explanation instead.

<span class="mw-page-title-main">Rodent</span> Order of mammals

Rodents are mammals of the order Rodentia, which are characterized by a single pair of continuously growing incisors in each of the upper and lower jaws. About 40% of all mammal species are rodents. They are native to all major land masses except for New Zealand, Antarctica, and several oceanic islands, though they have subsequently been introduced to most of these land masses by human activity.

<span class="mw-page-title-main">Lactation</span> Release of milk from the mammary glands

Lactation describes the secretion of milk from the mammary glands and the period of time that a mother lactates to feed her young. The process naturally occurs with all sexually mature female mammals, although it may predate mammals. The process of feeding milk in all female creatures is called nursing, and in humans it is also called breastfeeding. Newborn infants often produce some milk from their own breast tissue, known colloquially as witch's milk.

The Bruce effect, or pregnancy block, is the tendency for female rodents to terminate their pregnancies following exposure to the scent of an unfamiliar male. The effect was first noted in 1959 by Hilda M. Bruce, and has primarily been studied in laboratory mice. In mice, pregnancy can only be terminated prior to embryo implantation, but other species will interrupt even a late-term pregnancy.

<span class="mw-page-title-main">Parental brain</span>

Parental experience, as well as changing hormone levels during pregnancy and postpartum, cause changes in the parental brain. Displaying maternal sensitivity towards infant cues, processing those cues and being motivated to engage socially with her infant and attend to the infant's needs in any context could be described as mothering behavior and is regulated by many systems in the maternal brain. Research has shown that hormones such as oxytocin, prolactin, estradiol and progesterone are essential for the onset and the maintenance of maternal behavior in rats, and other mammals as well. Mothering behavior has also been classified within the basic drives. Less is known about the paternal brain, but changes in the father's brain occur alongside the mother once the offspring is born.

<span class="mw-page-title-main">Begging in animals</span>

Begging in animals is when an animal solicits being given resources by another animal. This is usually a young animal soliciting food from their parents, brood hosts or other adults. However, the resource is sometimes non-food related or may be solicited by adult animals. Begging behavior is most widely studied in birds, however, mammals, amphibians, and invertebrates perform begging displays. Generally in food solicitation, begging behavior is instinctive, although in some instances it is learned.

Social monogamy in mammals is defined as a long term or sequential living arrangement between an adult male and an adult female.

In biology, paternal care is parental investment provided by a male to his own offspring. It is a complex social behaviour in vertebrates associated with animal mating systems, life history traits, and ecology. Paternal care may be provided in concert with the mother or, more rarely, by the male alone.

Endocrinology of parenting has been the subject of considerable study with focus both on human females and males and on females and males of other mammalian species. Parenting as an adaptive problem in mammals involves specific endocrine signals that were naturally selected to respond to infant cues and environmental inputs. Infants across species produce a number of cues to inform caregivers of their needs. These include visual cues, like facial characteristics, or in some species smiling, auditory cues, such as vocalizations, olfactory cues, and tactile stimulation. A commonly mentioned hormone in parenting is oxytocin, however many other hormones relay key information that results in variations in behavior. These include estrogen, progesterone, prolactin, cortisol, and testosterone. While hormones are not necessary for the expression of maternal behavior, they may influence it.

Behavioural responses to stress are evoked from underlying complex physiological changes that arise consequently from stress.

Communal burrow refers to the habitat built by some species of mammals as a community habitat. There are some species that build burrows, but not communal burrows; and there are some species that live in communal groups, but do not construct burrows or any other type of habitat.

References

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  2. vom Saal, F.S.; Howard, L.S (1982), "The regulation of infanticide and parental behavior implications for reproductive success in male mice", Science, 215 (4537): 1270–1272, doi:10.1126/science.7058349
  3. Ebensperger, L.A. (1998), "Do female rodents use promiscuity to prevent male infanticide?", Ethology Ecology and Evolution, 10 (2): 129–141, doi:10.1080/08927014.1998.9522862
  4. Saltzman, W., Ahmed, S., Fahimi, A., Wittwer, D., & Wegner, F. (2006). Social suppression of female reproductive maturation and infanticidal behavior in cooperatively breeding Mongolian gerbils. Hormones and Behavior, 49, 527-537.
  5. Saltzman, W., Thinda, S., Higgins, A.L., Matsumoto, W.R., Ahmed, S., McGeehan, L., & Kolb, E.M. (2009). Effects of siblings on reproductive maturation and infanticidal behavior in cooperatively breeding Mongolian gerbils. Developmental Psychobiology, 51(1), 60-72.
  6. Heiming, R. S., Bodden, C., Jansen, F., Lewejohann, L., Kaiser, S., Lesch, K.-P., Palme, R., & Sachser, N. (2011). Living in a dangerous world decreases maternal care: A study in serotonin transporter knockout mice. Hormones and Behavior, 60(4), 397-407.
  7. Schneider, J. S., Stone, M. K., Wynne-Edwards, K. E., Horton, T. H., Lydon, J., O'Malley, B., & Levine, J. E. (2003). Progesterone receptors mediate male aggression toward infants. PNAS,100(5), 2951-2956.
  8. Holmes, W.G. (1977), "'Cannibalism in the arctic ground squirrel (Spermophilus parryii)", Journal of Mammalogy, 58 (3): 437–438., doi:10.2307/1379350, JSTOR   1379350
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  11. Blumstein, D.T. (2000). The evolution of infanticide in rodents: a comparative analysis. In: Infanticide by males and its implications (C. van Schaik and C.H. Janson, eds.). Cambridge, UK: Cambridge University Press.
  12. Ebensperger, L.A. (2001), "infanticide in the hystricognath rodent, Octodon degus: Does ecology play a role?", Acta Ethol., 3 (2): 89–93, doi:10.1007/s102110000032
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