Infanticidal Behavior Research Articles

Are age and sex differences in brain oxytocin receptors related to maternal and infanticidal behavior in naïve mice?

This article is part of a Special Issue “Parental Care”.There is significant variability in the behavioral responses displayed by naïve young and adult mice when first exposed to pups. This variability has been associated with differences in the expression of oxytocin receptors (OXTRs) in the brain in several species. Experiment I investigated the behavioral responses of juvenile, adolescent, and adult CB57BL/6 males and females when first exposed to pups. We found an age increase in maternal females (11% of juveniles, 20% of adolescents, and 50% of young adults), and infanticidal males (0% of juveniles, 30% of adolescents, 44.5% of young adults, and 100% of older adults). Experiment II investigated OXTR density in the brain of juvenile and adult mice. Our results revealed an age decline in the density of OXTR in several brain regions, including the lateral septum, cingulated and posterior paraventricular thalamic nucleus in both males and females. Adult females had higher OXTR density in the ventromedial nucleus/postero-ventral hypothalamus (VMH) and the accessory olfactory bulb (AOB), but lower density in the ventral region of the lateral septum (LSv) than juveniles. Males had lower OXTR density in the anterior olfactory area (AOA) compared to juveniles. No age or sex differences were found in the medial preoptic area, and amygdaloid nuclei, among other brain regions. This study suggests that 1) maturation of parental and infanticidal behavioral responses is not reached until adulthood; 2) the pattern of development of OXTR in the mouse brain is unique, region specific, and differs from that observed in other rodents; 3) either up or down regulation of OXTR in a few brain regions (VMH/AOB/LSv/AOA) might contribute to age or sex differences in parental or infanticidal behavior.

Why some male animals kill infants

Sexual Conflict![Figure][1] PHOTO: © [GEORGESANKER.COM][2]/ALAMY One of the most unpleasant aspects of social life in some animal species is killing of the young by adult males. Lukas and Huchard looked at mammalian groups with a variety of social systems—from mice to mongoose and from bats to bears. Infanticidal behavior in males appeared to be a result of sexual conflict in social species with nonseasonal breeding. Killing of a female's young by a new male will speed her return to a reproductive state and allow him to raise his own young. Evolutionarily, the only successful defense in females appears to be polyandry: Females that mate with multiple males make it hard for any one male to know that he is, or is not, the father of her offspring. Science , this issue p. [841][3] [1]: pending:yes [2]: http://GEORGESANKER.COM [3]: /lookup/doi/10.1126/science.1257226

Male attacks on infants and infant death during male takeovers in wild white‐headed langurs (Trachypithecus leucocephalus)

Infanticide was first observed in langurs nearly 50 years ago, and this rare phenomenon has been inferred to have either an evolutionarily adaptive function or to be a pathological and non-functional behavior. In this study, we report 5 male takeover events in one-male groups of white-headed langurs in the Nongguan Karst Hills, Guangxi, China from 1998 to 2006. We recorded 13 attacks on 9 infants by extra-group males or new resident males. During the male takeovers, all of the infants younger than 6 months (with an average age of 3.6 months [N = 11]) in the groups disappeared. The infant death rate during the 4.2 months after takeover by a new male was significantly higher than the infant death rate calculated for most of the year. Older infants that were still nursing (with an average age of 14.1 months [N = 7]) were often attacked and seriously wounded by the extra-group males or new resident males, but all of them survived. The interbirth intervals of females whose infants were assumed to be killed by males were significantly reduced relative to those of females in groups with stable male tenure (mean = 10 months vs 25 months). Our data suggest that males kill unrelated and unweaned infants during the takeover period to decrease the time until the infants' mothers resume fertility. Thus, infanticide would support sexual selection theory in white-headed langurs. The data also show that infanticidal behavior was directed toward the infants, especially those who were still nursing. Female dispersal may function as a counter-strategy to avoid infanticide.

Adult male coatis play with a band of juveniles

This study examined the play behaviour in one group of coatis (Nasua narica) at La Selva Biological Station in Costa Rica. We incidentally found adult males playing with juvenile coatis, and conducted post-hoc analyses to investigate this interaction. Coati groups consist of adult females and juveniles of both sexes until male juveniles reach two years of age and leave the band to become solitary. Adult males only tolerate juveniles for a brief period during breeding season when the males court females to mate. Outside of the breeding season, adult males are known to prey on juveniles. In this study, when adult males were present with the band, play occurred more than was expected by chance, and adult males engaged in many of these play bouts. Because the mechanisms driving infanticidal behaviour are not well understood, and adult male coatis show a range of behaviours from infanticide to highly affiliative interactions with juveniles, using coatis as a model system may elucidate mechanisms underlying infanticide.

New views on how population‐intrinsic and community‐extrinsic processes interact during the vole population cycles

Based on evidence from a series of recent studies linking behaviour to demography in experimental vole populations we propose how intrinsic and extrinsic factors interact through the various phases of the multi‐annual population cycles of voles and lemmings. We hypothesise that population growth in the increase phase of the cycle is enhanced by a high degree of space sharing (sociality) among reproductive females who share resource patches, especially during winter. These social females enjoy a high reproductive output due to good resource conditions, and facilitation provided by communal thermoregulation, breeding and defence of weanlings towards infanticidal conspecifics. We hypothesise on the other hand that the crash phase is initiated and enhanced by predation of adult males that leads to a series of cascading events involving infanticidal behaviour by immigrant males, increased mortality of adult social females, and inversely density‐dependent and/or disturbance‐induced dispersal. These events further enhance predation‐induced mortality and thus a negative feed‐back loop to the rate of the crash. In this framework we may explain how extrinsic factors such as predation and winter resource distribution contribute to transitions between docile and aggressive behaviours, and how this transition is spatially synchronised by inversely density‐dependent dispersal that may act to mediate a rapidly spreading wave throughout the population. We propose that innate differences among rodent species in their propensities for different social organizations also determine their propensity for exhibiting multi‐annual cycles as well as other cycle‐related phenomena such as shape of the population cycles and spatial synchrony. We provide a set of testable predictions for further empirical evaluation.

Advantage of rare infanticide strategies in an invasion experiment of behavioural polymorphism.

Killing conspecific infants (infanticide) is among the most puzzling phenomena in nature. Stable polymorphism in such behaviour could be maintained by negative frequency-dependent selection (benefit of rare types). However, it is currently unknown whether there is genetic polymorphism in infanticidal behaviour or whether infanticide may have any fitness advantages when rare. Here we show genetic polymorphism in non-parental infanticide. Our novel invasion experiment confirms negative frequency-dependent selection in wild bank vole populations, where resource benefits allow an infanticidal strategy to invade a population of non-infanticidal individuals. The results show that infanticidal behaviour is highly heritable with genetic correlation across the sexes. Thus, a positive correlative response in male behaviour is expected when selection operates on females only and vice versa. Our results, on one hand, demonstrate potential benefits of infanticide, and on the other, they open a new perspective of correlative evolution of infanticide in females and males.

Timing of oviposition enables dominant female burying beetles to destroy brood-parasitic young

Infanticide can increase an individual’s reproductive success through reduced competition for its offspring. Here we document the occurrence and effects of infanticidal behaviour by dominant female burying beetles, Nicrophorus vespilloides, in nontolerant breeding associations. Burying beetles feed and guard their young on buried carcasses, and on small carcasses, conspecific females engage in intense aggression. Dominants largely exclude subordinates from the carcass and are the sole caregivers for the larvae. Although subordinates and dominants produce similar egg clutches, only one out of five surviving offspring is the subordinate’s. We hypothesized that much of this skew is due to temporally cued infanticide by dominants. Females oviposit over the course of 24–48 h, and kill larvae they encounter prior to the hatching of their own larvae. Such infanticide can lead to significant skew only if the dominant’s larvae hatch significantly later than the subordinate’s, and if more subordinate than dominant larvae hatch during the infanticidal phase. The subordinate’s share of larvae hatching during the parental phase must be smaller than her share of eggs, and the portion of subordinate larvae killed by the dominant should increase with an increasing difference in oviposition time between the two females. These predictions were met. Dominant females, who had exclusive access to the carcass and larvae, were able to use temporal cues to destroy over half of the subordinates’ first-instar larvae. This is the first study to unambiguously document the primary mechanism underlying reproductive dominance in nontolerant associations of female N. vespilloides.

Extensive infanticide in enclosed European wild boars ( Sus scrofa)

Infanticidal behaviour, behaviour with wide welfare implications, is wide-spread among animals of various taxonomic groups, but has not previously been systematically studied in European wild boars, which are commonly kept in enclosures in Sweden and Finland for meat and recreation hunting. We studied the behaviour of wild boars in one enclosure during three reproductive seasons. Non-maternal infanticide was documented in 14 out of 22 litters, causing the deaths of all piglets in all but 1 affected litters. Infanticide was typically performed during or shortly after parturition by a sow which was older ( P < 0.05) and tended to be larger ( P = 0.068) than the victimised sow, and was not affected by whether or not the involved females were mother–daughter pairs. A questionnaire sent to 112 owners of a total of 116 enclosures in Sweden and Finland resulted in 62 valid responses. Non-maternal infanticide was reported to be the most common cause of piglet pre-weaning mortality, which in total (including all causes) was estimated to be 29.1%. The occurrence of infanticide was unrelated to size of enclosure (less or more than 20 ha) and to variations in supplementary feeding routines (less or more than once a week) ( P > 0.05), which may suggest that the behaviour could be a part of the normal behavioural repertoire in European wild boars. The observed levels of infanticide constitute a major welfare problem in captive wild boars.

Association and haplotype analysis of candidate genes in five genomic regions linked to sow maternal infanticide in a white Duroc × Erhualian resource population

BackgroundMaternal infanticide is an extreme and failed maternal behavior, which is defined as an active attack on piglets using the jaws, resulting in serious or fatal bite wounds. It brings big economic loss to the pig industry and severe problems to piglets' welfare. But little is known about the genetic background of this behavior. Quantitative trait loci (QTL) for maternal infanticide were identified in a White Duroc × Erhualian intercross by a non-parametric linkage analysis (NPL) in our previous study. In this study, associations of 194 microsatellite markers used in NPL analysis with maternal infanticide behavior were further analyzed by transmission-disequilibrium test (TDT). On this basis, seven genes (ESR2, EAAT2, BDNF, OXTR, 5-HTR2C, DRD1 and GABRA6) at five genomic regions were selected and further analyzed. Associations of single nucleotide polymorphisms (SNPs) and haplotypes in each gene with maternal infanticide behavior were evaluated.ResultsMicrosatellite markers on pig chromosome (SSC) 2, 13, 15, and X displayed significance at P < 0.05 by both TDT and NPL. Of the seven candidate genes, three ESR2 SNPs had nominal evidence for association (P < 0.05). Allele A at EAAT2 g. 233G > A and allele T at DRD1 g.1013C > G > T also showed evidence of overtransmission to infanticidal sows. In the overall tests of association of haplotypes, candidate genes of ESR2, EAAT2 and DRD1 achieved overall significance level (P < 0.05). Haplotype [A; A; G], [G; A; G], [A; G; G] and [C; C], respectively, from ESR2, EAAT2 and DRD1 showed higher frequencies to infanticidal sows (P < 0.05). Alleles among haplotypes and SNPs which showed an overtransmission to infanticidal sows were from White Duroc.ConclusionsFrom association tests of SNPs and haplotypes, ESR2, EAAT2 and DRD1 showed significant associations with maternal infanticide. This result supported the existence of QTL for maternal infanticide behavior on SSC1, SSC2 and SSC16.

Stability and potential inheritance of infanticidal behavior in prairie voles

Naïve female prairie voles show significant variability in their behavioral response to newborns. We investigated whether that behavioral response (a) was related to the quality of postpartum maternal behavior; (b) was affected by postpartum maternal experience; and (c) could be selectively bred. The behavior of females was recorded in three conditions: as naïve in a nonreproductive context, as single lactating (no male present), and as experienced mother in a nonreproductive context. Finally, females and males with similar behavioral response to newborns were selectively bred for three generation. Males were removed before the offspring was born. Our results revealed that (a) naïve females that attacked pups, spent more time distant from them after parturition than those that were maternal or ignored the pups (p < .05); (b) postpartum maternal experience did not reverse infanticidal behavior; and (c) at the third generation of selective breeding, 90% of the offspring of females that were nonmaternal as virgins, behaved as their mothers. These findings suggest that the infanticidal behavioral response is a stable behavioral trait and might be passed to the offspring.

Is Mating Alone Enough to Inhibit Infanticide in Male Bank Voles?

AbstractInfanticide, the killing of conspecific young, is commonly recognized as an adaptive behavioural strategy enhancing the fitness of the perpetrator. Infanticide is supposed to be inhibited in several male rodent species after mating with a time lag to the time when perpetrators own offspring would be born. This is because males with no parental care do not recognize their own offspring. It has been suggested that copulation alone is enough to inhibit infanticidal behaviour in male rodents. Infanticidal behaviour occurs in more than 50% of male bank voles (Myodes glareolus), and offspring loss because of infanticide may have a great effect on breeding success and population recruitment. In a laboratory experiment, we studied whether infanticidal male bank voles after successful mating stop the killing of pups. Infanticidal males were paired with a female until successful copulation. After the young were born, the males’ infanticidal behaviour was studied from the time of expected birth of own pups until their post‐weaning age. We predicted that mated infanticidal males are inhibited from committing infanticide especially during the time period when pups are less than 10 d old. Against our prediction, 67% of the infanticidal males continued the killing of pups in the age of 3 d. Infanticidal behaviour remained stable, and half of the males were infanticidal still at the age of weaning of pups. Our results are contradictory to previous studies, as we observed no inhibition of infanticide during early life of pups nor increase in infanticide again when their own offspring would have reached the ‘safe’ age and size after weaning. We suggest that mating alone is not sufficient to inhibit infanticide. Thus, we suggest that other cues of the female with whom the male mated with or on her territory are needed for inhibition to occur.

Infanticide in Cercopithecus mitis stuhlmanni in the Kakamega Forest, Kenya: Variation in the Occurrence of an Adaptive Behavior

Infanticide by males is widespread across mammals and especially prevalent among primates. Considerable research has examined how fitness benefits can explain the occurrence of this behavior; less is known, however, about intrapopulation variation in its occurrence. We evaluated 10 infanticides by males in wild blue monkeys according to the sexual selection hypothesis. To explore intrapopulation variation in occurrence of infanticide, we compared these cases to 38 cases that were contextually similar but in which infanticide did not occur. We examined male reproductive benefit, infant age, maternal parity, postconception estrus, group defense, available mating partners, and context of takeover. We based comparisons on daily or near daily records of male presence in the study groups, infant birth dates, and male-female sexual interactions. Infanticides followed predictions of the sexual selection hypothesis: males were unlikely to kill their own offspring, the period for the mother’s return to conception was reduced by half, and males increased their chance of siring her next offspring. Difference in male reproductive benefit, costs, and motivation did not fully explain the observed variation in infanticide occurrence. Infants were more likely to be spared if they were older when a male first arrived, or if their mother had mated with the male in the second month after conception. The most important determinant of infant fate, however, was male identity, a finding consistent with 2 scenarios: 1) an infanticidal tendency may be influenced by a genetic polymorphism that is not fixed in this population or 2) infanticidal behavior may be a conditional male strategy. Further research on intrapopulation variation in infanticidal behavior should focus especially on characteristics of males.

D2 antagonist during development decreases anxiety and infanticidal behavior in adult female prairie voles (Microtus ochrogaster)

On postnatal day 8, prairie vole pups were randomly assigned a treatment of 1mg/kg SKF38393 (D1 agonist), quinpirole (D2 agonist), SCH23390 (D1 antagonist), eticlopride (D2 antagonist), or saline vehicle. As adults, females treated with eticlopride exhibited reduced anxiety-like behavior in an elevated plus maze and a reduction in infanticidal behavior. These behavioral effects were not seen in males. These data demonstrate that a single exposure to a D2 antagonist during development can have persistent, sex-specific effects on behavior into adulthood.

Nest intrusion and infanticidal attack on nestlings in great cormorants Phalacrocorax carbo: why do adults attack conspecific chicks?

Infanticide, the killing of young animals by conspecifics, has been observed in diverse taxa. The function of infanticide has been classified as exploitation, sexual selection, parental manipulation or resource competition. We observed infanticidal behavior and its reproductive results at five breeding colonies of great cormorants from January to August 2008. Eighteen cases of nest intrusions and/or attacks toward a chick by conspecific non-nest-owners were observed, and two of them were filmed. In both attacks, perpetrators pecked the necks of chicks several times with display. The chicks bent their necks down onto the nest and remained stationary. Our data did not support the exploitation hypothesis because adult cormorants did not use chicks as food. In addition, the perpetrators were not true parents and did not mate with the female nest owner, indicating that parental manipulation and sexual selection hypotheses were unlikely explanations. On the other hand, concurrent presence of adults during prelaying and chick-rearing periods at a particular colony affected the occurrence of nest takeovers and intrusions and/or attacks, suggesting that some conflicts over nests arise between individuals that are at different stages of the breeding cycle. Digital videos relating to this article are available at http://www.momo-p.com/showdetail-e.php?movieid=momo090421pc01a and http://www.momo-p.com/showdetail-e.php?movieid=momo090421pc02a.

Polyandry enhances offspring survival in an infanticidal species

The adaptive significance of polyandry is an intensely debated subject in sexual selection. For species with male infanticidal behaviour, it has been hypothesized that polyandry evolved as female counterstrategy to offspring loss: by mating with multiple males, females may conceal paternity and so prevent males from killing putative offspring. Here we present, to our knowledge, the first empirical test of this hypothesis in a combined laboratory and field study, and show that multiple mating seems to reduce the risk of infanticide in female bank voles Myodes glareolus. Our findings thus indicate that females of species with non-resource based mating systems, in which males provide nothing but sperm, but commit infanticide, can gain non-genetic fitness benefits from polyandry.

Effects of progesterone on male-mediated infant-directed aggression

Many species that engage in parental behavior exhibit infanticide under certain circumstances. The neural signals regulating the transition from infant care giver to infant killer and back remain unclear. Previously we demonstrated that progesterone (P) and its receptor (PR) have inhibitory effects on parental behavior and increase infant-directed aggression in male mice. In the present studies we sought to elucidate the mechanisms by which the effects of P are manifested. Because the onset of parental behavior in females is associated with the withdrawal of P at the end of pregnancy we tested the hypothesis that withdrawal of P would similarly enhance parental behavior in males. Virgin male mice were implanted with P or vehicle for 21 days, replicating the duration of pregnancy in females. Tests were run for parental and infanticidal behavior 5 days after removal of the capsules. P increased the proportion of nonparental males that attacked pups. However, neither the number of males exhibiting parental care nor the quality of care was affected by P treatment. Serum P and testosterone (T) levels were not different from controls at the time of behavioral testing indicating continued elevations in peripheral hormones are not required for the expression of infanticide. In conclusion, withdrawal of P does not trigger the onset of parental behavior in males. Rather, prior exposure to P induces persistent infanticidal behavior in adult male mice.

Male pheasant‐tailed jacanas commit infanticides to avoid cuckoldry when paternity of eggs is doubtful

Many hypotheses have been proposed to explain infanticide, killing the young or destruction of eggs by conspecific adults. We report cases of infanticide in the polyandrous pheasant‐tailed jacana (Hydrophasianus chirurgus) of Taiwan. In 2004, three males and one female bred at our study site. The female mated with the three males sequentially and laid clutches for all of them. Infanticidal behaviour was observed in all males and in all but one clutch, the first clutch of the breeding season. The infanticidal males threw out the first one or two eggs of a clutch, but then accepted replacement eggs and incubated normally. Because the intervals between copulation with different males were short (1–10 days) and sperm can remain viable within the female reproductive tract for at least 4–5 days, sperm competition among the males may have been intense, and the paternity of the first few eggs in each clutch was doubtful. We suggest that male pheasant‐tailed jacana may use infanticide as a strategy to avoid cuckoldry when the paternity of eggs is in doubt.

Effects of siblings on reproductive maturation and infanticidal behavior in cooperatively breeding Mongolian gerbils.

Mongolian gerbils living with their natal families undergo delayed reproductive maturation while helping to rear their younger siblings, whereas those housed away from their natal families may mature earlier but often respond aggressively to unfamiliar pups. We tested whether cohabitation with pups contributes to reproductive suppression and inhibition of infanticidal behavior, using young males and females housed with (1) their parents and younger siblings (pups), (2) parents without pups, (3) mixed-sex littermate groups, or (4) mixed-sex groups of unrelated peers. Maturation in males was inhibited by cohabitation with the parents, while maturation in females was further suppressed in the presence of pups. Males in all housing conditions showed little aggression towards unfamiliar pups, whereas females were usually infanticidal unless housed with pups. Aggression toward pups was especially pronounced in females that were pregnant or undergoing ovulatory cycles. Thus, cohabitation with younger siblings may intensify reproductive suppression and inhibit infanticidal behavior in female gerbils, whereas male gerbils exhibit parentally induced reproductive suppression and low rates of infanticide even in the absence of younger siblings.

Infanticide and Maternal Offspring Defence in European Rabbits under Natural Breeding Conditions

AbstractInfanticide is an important source of mortality of dependent offspring in several mammal species, whereas female conspecifics are often the perpetrators. This has led to maternal counter‐strategies, such as the defence of the nests. However, cases of infanticide are hard to detect in the field, and studies on maternal offspring defence behaviour under natural breeding conditions are scarce. We conducted such a study on the European rabbit (Oryctolagus cuniculus), which is usually considered to show low maternal care. The study was carried out over 5 yr on a field enclosure population. We (1) studied infanticide rates and the impact of potential determinants: the group density and age structure of the females’ rank hierarchy within the groups; we used the latter as an estimator of social group stability. We (2) studied if mothers defend their breeding burrow against approaching, potentially infanticidal females. Overall, we recorded infanticide in 5% of all litters; infanticide was the cause in 12% of cases of litter mortality. The proportion of infanticide was 7% higher in groups where same‐age females occupied successive rank positions than in groups where the females’ rank hierarchy had a more heterogeneous and linear age structure. We hypothesize that social instability in the former groups was the reason for the increased infanticide risk. Infanticide rates were not correlated with group density and did not differ among mothers with different social ranks. Infanticide occurred exclusively during the first 10 d after parturition. During this time, mothers stayed closer to their breeding burrows than shortly before parturition or during later lactation. Moreover, mothers were more aggressive against other females in proximity to their breeding burrow than in more distant areas. We suggest that the pattern of spacing behaviour and intrasexual aggression of rabbit mothers are an adaptive response to the occurrence of female infanticidal behaviour.

Infanticidal Behavior in the Subsocial Beetle Odontotaenius disjunctus (Illiger) (Coleoptera: Passalidae)

Infanticide, the killing of young, reproductively immature individuals of the perpetrator's same species, has many interesting implications for reproductive fitness. Here we provide the first experimental description of infanticidal behavior in the passalid beetle Odontotaenius disjunctus (Illiger). To test our hypothesis that infanticide is triggered by the takeover of burrows by adults that had yet to reproduce in the mating season, we measured the mortality of larvae when housed with adults that were reproducing or had not yet reproduced. A significantly higher mortality was observed in larvae housed with adults that had not reproduced than when housed with their own parent or with unrelated reproducing adults. Infanticidal behavior of O. disjunctus is thought to result from the reproductive advantage obtained by taking over an existing burrow and thereby securing one with high food resource quality.