Infanticide (zoology)

In animals, infanticide involves the killing of young offspring by a mature animal of its own species, and is studied in zoology, specifically in the field of ethology. Ovicide is the analogous destruction of eggs. Although human infanticide has been widely studied, the practice has been observed in many other species throughout the animal kingdom. These include microscopic rotifers, insects, fish, amphibians, birds and mammals.Hoogland, J. L. (1985) Infanticide in Prairie Dogs: Lactating Females Kill Offspring of Close Kin "Science" 230:1037-1040.] Infanticide can be practiced by both males and females.

Infanticide caused by sexual conflict has the general theme of the killer (often male) becoming the new sexual partner of the victim's parent which would otherwise be unavailable to it. This represents a gain in fitness by the killer, and a loss in fitness by the parents of the offspring killed. This is a type of evolutionary struggle between the two sexes, in which the victim sex may have its own counter-adaptations which reduce the success of this practice. It may also occur for other reasons, such as the struggle for food between females. In this case individuals may even kill closely related offspring.

Filial infanticide occurs when a parent kills its own offspring. This often involves consumption of the young themselves, which is termed filial cannibalism. The behavior is widespread in fishes, and is seen in terrestrial animals as well. Human infanticide has been recorded in almost every culture. A unique aspect of human infanticide is selective killing based on gender.

Background

Infanticide only came to be seen as a significant occurrence in nature quite recently. At the time it was first seriously treated by Yukimaru Sugiyama, [Sugiyama, Y. (1965) On the social change of Hanuman langurs ("Presbytis entellus") in their natural conditions. "Primates" 6:381-417.] infanticide was attributed to stress causing factors like overcrowding and captivity, and was considered pathological and maladaptive. Classical ethology held that conspecifics (members of the same species) rarely killed each other. [Lorenz, K. (1966) "On Aggression". New York: Harcourt, Brace and World.] By the 1980s it had gained much greater acceptance. Possible reasons it was not treated as a serious natural phenomenon include its abhorrence to people, the popular group and species selectionist notions of the time (the idea that individuals behave for the good of the group or species; compare with gene-centered view of evolution), and the fact that it is very difficult to observe in the field. [Hausfater, G. & S. B. Hrdy (1984) "Infanticide: Comparative and evolutionary perspectives" New York, Aldine. 598 p. ISBN 0202020223]

Infanticide involving sexual conflict

This form of infanticide represents a struggle between the sexes, where one sex exploits the other, much to the latter's disadvantage. It is usually the male who benefits from this behavior, though in cases where males play similar roles to females in parental care the victim and perpetrator may be reversed (see Bateman's principle for discussion of this asymmetry).

By males

Hanuman langurs (or gray langurs) are an Old World monkey found in India. They are a social animal, living in groups. Each group is generally dominated by a single male, with many females, though the male must struggle for control of the group with other males. When a male tries to take over a group, there is a violent struggle with the existing male. If successful in overthrowing the previous male, infants of the females are then killed. [Hrdy, D. B. (1977) Infanticide as a primate reproductive strategy. "American Scientist". 65:40-49] This infanticidal period is limited to the window just after the group is taken over. Cannibalism has not been observed in this species, however.

This behavior not only reduces intraspecific competition between the incumbent's offspring and those of other males and increases the parental investment afforded to their own young, but also allows females to become sexually receptive sooner. This is because females of this species, as well as many other mammals, do not ovulate during the period in which they produce milk. It then becomes easier to see how this behavior could have evolved. If a male kills a female's young, they stop lactating and are able to become pregnant again. As males are in a constant struggle to protect their group, those that express infanticidal behavior will contribute a larger portion to future gene pools (see natural selection).

Similar behavior is also seen in male lions, among other species, who also kill young cubs, allowing them to impregnate the females. Unlike langurs, male lions live in small groups, which cooperate to take control of a pride from an existing group.Pusey, A. E., and C. Packer. (1994) Infanticide in lions. In Parmigiani, S. and F. S vom Saal (editors)"Infanticide and parental Care" Harwood Academic Press, Chur, Switzerland.] They will attempt to kill any cubs that are roughly 9 months old or less, though as in other species, the female will attempt to defend their cubs viciously. Males have, on average, only a two year window in which to pass on their genes, and female lions only give birth once every two years, so the selective pressure from them to behave like this is strong. In fact it is estimated that a quarter of cubs dying in the first year of their life are victims of infanticide.

Male mice show great variation in behavior over time. After fertilizing a female, they become aggressive towards mouse pups for three weeks, killing any they come across. After this period however, their behavior changes dramatically, and they become paternal, caring for their own offspring. This lasts for almost two months, but afterwards they become infanticidal once more. It is no coincidence here that the female gestation period is three weeks as well, or that it takes roughly two months for pups to become fully weaned and leave their nest. The proximate mechanism that allows for the correct timing of these periods involves circadian rhythms (see chronobiology), each day and night cycle affecting the mouse's internal neural physiology, and disturbances in the duration of these cycles results in different periods of time between behaviors. [Perrigo, G., W. C. Bryant & F. S. vom Saal (1990) A unique neural timing system prevents male mice from harming their own offspring. "Animal Behavior" 39:535-539.] The adaptive value of this behavior switching is twofold; infanticide removes competitors for when the mouse does have offspring, and allows the female victims to be impregnated earlier than if they continued to care for their young, as mentioned above.

Gerbils, on the other hand, no longer commit infanticide once they have paired with a female, but actively kill and eat other offspring when young. The females of this species behave much like male mice, hunting down other litters except when rearing their own. [Hausfater, G. (1984) Infanticide: Comparative and Evolutionary Perspectives "Current Anthropology" 25:500-502.]

Prospective infanticide

Prospective infanticide is a subset of sexual competition infanticide in which young born "after" the arrival of the new male are killed. This is less common than infanticide of existing young, but can still increase fitness in cases where the offspring could not possibly have been fathered by the new mate, i.e. one gestation or fertility period. This is known to occur in lions and langurs, and has also been observed in other species such as house wrens.Freed, L. A. (1987) Prospective Infanticide and Protection of Genetic Paternity in Tropical House Wrens "The American Naturalist" 130:948-954.] In birds, however, the situation is more complex, as female eggs are fertilized one at a time, with a 24-hour delay between each. Males may destroy clutches laid 12 days or more after their arrival, though their investment of around 60 days of parental care is large, so a high level of parental certainty is needed.

By females

Females are also known to display infanticidal behavior. This may appear unexpected, as the conditions described above do not apply. Males are not always an unlimited resource though - in some species, males provide parental care to their offspring, and females may compete indirectly with others by killing their offspring, freeing up the limiting resource that the males represent. This has been documented in research by Stephen Emlen and Natalie Demong on wattled jacanas ("Jacana jacana"), a tropical wading bird. [Emlen, S. T., N. J. Demong, and D. J. Emlen (1989) Experimental induction of infanticide in female wattled jacanas. "Auk". 106:1-7.] With the wattled jacana, it is exclusively the male sex which broods, while females defend their territory. In this experiment Demong and Emlen found that removing females from a territory resulted in nearby females attacking the chicks of the male in most cases, evicting them from their nest. The males then fertilized the offending females and cared for their young. [For footage of this, see Attenborough, D. (1990) "The Trials of Life", Episode 12, or "Evolution", Episode 3 "Why Sex?".] Emlen describes how he "shot a female one night, and [...] by first light a new female was already on the turf. I saw terrible things—pecking and picking up and throwing down chicks until they were dead. Within hours she was soliciting the male, and he was mounting her the same day. The next night I shot the other female, then came out the next morning and saw the whole thing again." [cite web
url=http://discovermagazine.com/1996/sep/firstkillthebabi864
title=First, Kill the Babies
accessdate=2008-01-19
author=Zimmer, Carl
date=1996-09-01
work=Discover]

Infanticide is also seen in giant water bugs.Ichikawa, N. (1995) Male counterstrategy against infanticide of the female giant water bug "Lethocerus deyrollei" (Hemiptera: Belostomatidae). "Journal of Insect Behavior" 8:181-186.] "Lethocerus deyrollei" is a large and nocturnal predatory insect found in still waters near vegetation. In this species the males take care of masses of eggs by keeping them hydrated with water from their bodies. Without a male caring for the eggs like this, they become desiccated and will not hatch. In this species males are a scarce resource which females must sometimes compete for. Those that cannot find a free male will often stab the eggs of a brooding one. As in the above case, males then fertilize this female and care for her eggs. Noritaka Ichikawa has found that males only moisten their eggs during the first 90 seconds or so, after which all of the moisture on their bodies has evaporated. However, they guard the egg masses for as long as several hours at a time, when they could be hunting prey. They do not seem to prevent further evaporation by staying guard, as males that only guarded the nest for short periods were seen to have similar hatching rates in a controlled experiment where there were no females present. It seems rather that males are more successful in avoiding infanticidal females when they are out of the water with their eggs, which might well explain the ultimate cause of this behavior.

Resource competition

Black-tailed prairie dogs are colonially-living, harem-polygynous squirrels found mainly in the United States. Their living arrangement involves one male living with four or so females in a territory defended by all individuals, and underground nesting. Black-tails only have one litter per year, and are in estrous for only a single day around the beginning of spring.

A seven-year natural experiment by John Hoogland and others from the University of Princeton revealed that infanticide is widespread in this species, including infanticide from invading males and immigrant females, as well as occasional cannibalism of an individual's own offspring. The surprising finding of the study was that by far the most common type of infanticide involved the killing of close kin's offspring. This seems illogical, as kin selection favors behaviors that promote the well-being of closely related individuals. It was postulated that this form of infanticide is more successful than trying to kill young in nearby groups, as the whole group must be bypassed in this case, while within a group only the mother need be evaded. Marauding behavior is evidently adaptive, as infanticidal females had more and healthier young than others, and were heavier themselves as well. This behavior appears to reduce competition with other females for food, and future competition among offspring.

Similar behavior has been reported in the meerkat ("Suricata suricatta"), including cases of females killing their mother's and daughter's offspring. Infanticidal raids from neighboring groups also occurred. [Clutton-Brock, T. H. "et al" (1998) Infanticide and Expulsion of Females in a Cooperative Mammal "Proceedings: Biological Sciences" 265:2291-2295.]

Costs and defenses

Costs of the behavior

While it may be beneficial for some species to behave this way, infanticide is not without risks to the perpetrator. Having already exhausted energy and perhaps sustained serious wounds in a fight with another male, attacks from females who vigorously defend their offspring may be telling for harem-polygynous males, with a risk of infection. It is also energetically costly to pursue a mother's young, which may try to escape.

Costs of the behavior described in prairie dogs include the risk to an individual of losing their own young while killing another's, not to mention the fact that they are killing their own relatives. In a species where infanticide is common, perpetrators may well be victims themselves in the future, such that they come out no better off; but as long as an infanticidal individual gains in reproductive output by its behavior, it will tend to become common. Further costs of the behavior in general may be induced by counter-strategies evolved in the other sex, as described below.

As a cost of social behavior

Taking a broader view of the black-tailed prairie dog situation, infanticide can be seen as a cost of social living. If each female were to have her own private nest away from others, she would be much less likely to have her infants killed when absent. This, and other costs such as increased spread of parasites, must be made up for by other benefits, such as group territory defense and increased awareness of predators.

An avian example published in "Nature" is acorn woodpeckers. Females nest together, possibly because those nesting alone have their eggs constantly destroyed by rivals. Even so, eggs are consistently removed at first by nest partners themselves, until the entire group lays on the same day. They then cooperate and incubate the eggs as a group, but by this time a significant proportion of their eggs have been lost because of this ovicidal behavior. [Mumme, R. L., W. D. Koenig, F. A. Pitelka. (1983) Reproductive competition in the communal acorn woodpecker: Sisters destroy each other's eggs. "Nature" 306:583-584.]

Counter-strategies

Because this form of infanticide reduces the fitness of killed individuals' parents, animals have evolved a range of counter-strategies against this behavior. These may be divided into two very different classes - those which tend to prevent infanticide, and those which minimize losses.

Loss minimization

Some females abort or resorb their own young while they are still in development after a new male takes over; this is known as the Bruce effect. [Bruce, H. M. (1959) An exteroceptive block to pregnancy in the mouse "Nature" 184:105.] This may prevent their young from being killed after birth, saving the mother wasted time and energy. However, this strategy also benefits the new male. In mice this can occur by the proximate mechanism of the female smelling the odor of the new male's urine. [Labov, J. B. (1981) Pregnancy blocking in rodents: Adaptive advantages for females. "American Naturalist" 18:361-371.]

Preventative adaptations

Infanticide in burying beetles may have led to male parental care. [Scott, M. P. (1990) Brood guarding and the evolution of male parental care in burying beetles. "Behavioral Ecology and Sociobiology" 26:31-40.] In this species males often cooperate with the female in preparing a piece of carrion, which is buried with the eggs and eaten by the larvae when they hatch. Males may also guard the site alongside the female. It is apparent from experiments that this behavior does not provide their young with any better nourishment, nor does is it of any use in defending against predators. However, other burying bugs may try to take their nesting space. When this occurs, a male-female pair is over twice as successful in nest defense, preventing the ovicide of their offspring.

Female langurs may leave the group with their young alongside the outgoing male, and others may develop a "false estrous" and allow the male to copulate, deceiving him into thinking she is actually sexually receptive. [Hrdy, S. B. (1977) "The Langurs of Abu" Harvard University Press, Cambridge, MA.] Females may also have sexual liaisons with other males. This promiscuous behavior is adaptive, because males will not know whether it is their own offspring they are killing or not, and may be more reluctant or invest less effort in infanticide attempts. [Agrell, J.; Wolff, J.; Ylönen, H. (1998) Counter-Strategies to Infanticide in Mammals: Costs and Consequences "Oikos" 83:507-517.] Lionesses cooperatively guard against scouting males, and a pair were seen to violently attack a male after it killed one of their young. [Packer, C., Pusey, A. (1983) Adaptations of female lions to infanticide by incoming males "The American Naturalist" 121:716-728] Resistance to infanticide is also costly, though: for instance, a female may sustain serious injuries in defending her young. At times it is simply more advantageous to submit than to fight. [Yamamura, N.; Hasegawa, T.; Ito, Y. (1990) Why Mothers Do Not Resist Infanticide: A Cost-Benefit Genetic Model "Evolution" 44:1346-1357.]

Filial infanticide

Filial infanticide occurs when a parent kills its own offspring. Both male and female parents have been observed to do this, as well as sterile worker castes in some eusocial animals.

Maternal

Maternal infanticide occurs when newborn offspring are killed by their mother. This is sometimes seen in pigs, [http://mark.asci.ncsu.edu/NCPorkConf/2002/lay.htm North Carolina Pork Conference] notes. 2002. North Carolina State University.] a behavior known as savaging which affects up to 5% of gilts. Similar behavior has been observed in various animals such as rabbits [Boyd, I. L. (1985) Investment in Growth by Pregnant Wild Rabbits in Relation to Litter Size and Sex of the Offspring "The Journal of Animal Ecology" 54:137-147] and burying beetles. [Trumbo, S. (1994) Interspecific Competition, Brood Parasitism, and the Evolution of Biparental Cooperation in Burying Beetles "Oikos" 69: 241-249.]

Paternal

Paternal infanticide—where fathers eat their own offspring—may also occur. When young bass hatch from the spawn, the father guards the area, circling around them and keeping them together, as well as providing protection from would-be predators. After a few days, most of the fish will swim away. At this point the male's behavior changes: instead of defending the stragglers, he treats them as any other small prey, and eats them.M. A. Elgar and Bernard J. Crespi (eds.). 1992. "Cannibalism: Ecology and Evolution of Cannibalism among Diverse Taxa" Oxford University Press, New York. (361pp) ISBN 0198546505]

Other

Honey bees may become infected with a bacterial disease called foul brood, which attacks the developing bee larva while still living in the cell. Some hives however have evolved a behavioral adaptation that resists this disease: the worker bees selectively kill the infected individuals by removing them from their cells and tossing them out of the hive, preventing it from spreading. The genetics of this behavior are quite complex. Experiments by Rothenbuhler showed that the 'hygienic' behavior of the queen was lost by crossing with a non-hygienic drone. This means that the trait must be recessive, only being expressed when both alleles contain the gene for hygienic behavior. Furthermore, the behavior is dependent on two separate loci. A backcross produced a mixed result. The hives of some offspring were hygienic, while others were not. There was also a third type of hive where workers removed the wax cap of the infected cells, but did nothing more. What was not apparent was the presence of a fourth group who threw diseased larvae out of the hive, but did not have the uncapping gene. This was suspected by Rothenbuhler however, who manually removed the caps, and found some hives proceeded to clear out infected cells. [Summarized in Dawkins, R. 1976. "The Selfish Gene" Oxford University Press. ISBN 0-19-286092-5] [Rothenbuhler, W. C. (1964) Behavior genetics of nest cleaning in honey bees. IV. Responses of F₁ and backcross generations to disease killed brood. "American Zoologist". 4:111-123.]

Humans and infanticide

Perceptions and importance

Like many of the darker aspects of nature, infanticide is a subject that many find discomforting. Cornell University ethologist Glenn Hausfater states that "infanticide has not received much study because it's a repulsive subject [...] Many people regard it as reprehensible to even think about it."

Research into infanticide in animals is in part motivated by the desire to understand human behaviors, such as child abuse. Hausfater explains that researchers are "trying to see if there's any connection between animal infanticide and child abuse, neglect and killing by humans [...] We just don't know yet what the connections are." [cite web|url=http://query.nytimes.com/gst/fullpage.html?sec=health&res=9401EFD81E39F934A2575BC0A964948260 |title=INFANTICIDE: ANIMAL BEHAVIOR SCRUTINIZED FOR CLUES TO HUMANS |author=Bayard Webster|year =1982|publisher="The New York Times"|accessdate=2008-01-18]

Infanticide by humans

Infanticide has been, and still is, practiced by some cultures, groups, or individuals. It is often, but not always, the mother who commits the act. In many past societies, certain forms of infanticide were considered permissible, whereas in most modern societies the practice is considered immoral and criminal. Nonetheless, it still takes place — in the Western world usually because of the parent's mental illness or violent behavior, and in some poor countries as a form of population control, sometimes with tacit societal acceptance. Female infanticide, a form of sex-selective infanticide, is more common than the killing of male offspring.

ee also

*Concealed ovulation (the evolution of which may be a counter-adaptation to infanticide by males)
*Parent-offspring conflict
*Parricide
*Runt
*Sexual cannibalism
*Sexual selection
*Siblicide
*Sociobiology

Further reading

*Hausfater, G. & S. B. Hrdy (1984) "Infanticide: Comparative and evolutionary perspectives" New York, Aldine. 598 p. ISBN 0202020223
*Parmigiani, S. & F. S. vom Saal (1994) "Infanticide and parental care" London: Harwood. 493 p. ISBN 9783718655052
*C. P. van Schaik & C. H. Janson (2000) "Infanticide by males and its implications" Cambridge University Press. 569 p. ISBN 0521772958

References

;General
*Alcock, J. (1998) "Animal Behavior: An Evolutionary Approach" (6th edition). Sinauer Associates, Inc. Sunderland, Massachusetts. ISBN 0-87893-009-4;Specificrefend