Changes in incidence of infanticidal and parental responses during the reproductive cycle in male and female wild mice Mus musculus

Most studies of infanticide in rodents have been carried out on laboratory animals. In the present study, pairs of infanticidal male and female wild mice were observed for changes in their responsiveness to alien pups during the reproductive cycle. Females killed pups during pregnancy, adopted alien pups during the lactation period, and killed pups again a month after the weaning of their offspring. In males, the transition from infanticidal to parental responses occurred as early as the first half of their mates' pregnancy, and only half of them resumed infanticide a month after the weaning of their litters. Subsequent experiments showed that two independent factors, the experience of copulation and cues from the pregnant female, accounted for the cessation of infanticide and onset of parental care in the male. The adaptive value of the co-existence of multiple mechanisms underlying the cessation of infanticide in male and female house mice is discussed with respect to the social life of this species.     

Hormonal Responses of Male Gerbils to Stimuli from Their Mate and Pups

Following copulation and cohabitation with a pregnant female, male gerbils show high levels of parental behavior toward their pups. The initiation of male parental behavior may be the result of neuroendocrine changes induced by cohabiting with the pregnant female or by pup stimuli. Experiment 1 examines the changes in androgen and prolactin levels in male gerbils cohabiting with females over the reproductive cycle. Gerbils were mated and blood samples taken from males for hormone analysis 1, 10, and 20 days after pairing and 3, 10, and 20 days after pups were born. A group of unmated male gerbils served as controls. Plasma prolactin levels of males were elevated throughout the female's pregnancy and lactation periods, but were only statistically significantly higher than those of unmated males 20 days after pups were born. Androgen levels rose during pregnancy and dropped significantly after the birth of the pups. These hormonal changes are similar to those found in males of monogamous birds and differ from those found in males of polygynous rodents such as the rat. Experiment 2 examined the hormonal responses of male and female gerbils to pup replacement after 4 hr of parent–pup separation. Female gerbils showed a significant elevation of prolactin levels 1 hr after pup replacement, but males did not. Males with pups returned showed no difference in androgen levels from males who did not have pups returned. Thus, male gerbils show neuroendocrine changes following long-term cohabitation with their mate and pups, but do not show acute hormone responses to pup removal and replacement. These results indicate that parental males have neuroendocrine changes associated with parental behavior and these differ from the neuroendocrine changes underlying female parental behavior.     

What Hanuman langur males know about female reproductive status

In species with a high risk of infanticide, a conflict of interest exists between the sexes over the amount of paternity information that is available to males. While females are expected to keep males unaware of their reproductive status in order to confuse paternity, selection should favor those male traits that enhance the males' assessment of female status and consequently of paternity probability. In Hanuman langurs (Semnopithecus entellus), a species that is extremely vulnerable to infanticide, females have been shown to successfully conceal the exact timing of ovulation from males--perhaps because they exhibit no sexual swelling and mate during all reproductive phases, including gestation. Nevertheless, it remains unclear whether males have hitherto unrecognized information about females' reproductive condition on a broader level that could still enhance male reproductive success. We investigated male assessment of female reproductive states in a population of wild Hanuman langurs as indicated by changes in male behavior, such as rates of copulations, anogenital inspections, and consortships, in relation to different female receptive periods (pregnant, fertile-nonconceptional, and conceptional). Our data indicate that males were able to discern qualitatively distinct reproductive states. Males were more interested in fertile than pregnant females, as indicated by higher copulation rates. Based on consortships, males distinguished fertile from nonfertile phases, as well as fertile, nonconceptional receptive periods from conceptional ones. Hanuman langur males are thus not as unaware of female reproductive condition as previously thought, supporting the idea of an ongoing battle of the sexes over paternity information. However, granting some knowledge while at the same time concealing the exact day of ovulation may also reflect a pure female strategy of balancing paternity concentration with paternity confusion, which is the most likely strategy in this system with high infanticide risk and male defense of infants.     

Oxytocin inhibits infanticide in female house mice (Mus domesticus)

Between 60 and 90% of female house mice spontaneously kill unrelated young. A previous report indicated that subcutaneous administration of oxytocin significantly reduced the frequency of infanticide by virgin and pregnant females. However, in this study a distinction could not be made between an action of oxytocin on the CNS versus a secondary effect such as an enhanced release of prolactin by oxytocin. In the current experiment, oxytocin administered intracerebroventricularly was equally as effective at inhibiting infanticide as sc oxytocin. There was no difference in the effectiveness of oxytocin between groups of infanticidal females that were gonadally intact, ovariectomized, or estrogen treated. Pretreatment of infanticidal females with the prolactin inhibitors, bromocriptine and cysteamine, was also without effect on the ability of oxytocin to inhibit infanticide. Last, prolactin-inhibiting drugs had no significant effect on spontaneous parenting behavior by female mice. These data suggest that oxytocin acts directly on the CNS to alter behavior toward pups and that prolactin may not play a role in the maternal behavior of the house mouse.     

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

Infanticide, 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.     

Neurological effects of aromatase deficiency in the mouse

In the brain, the conversion from androgen into estrogen is an important process for the differentiation of the brain function in male rodents. The aromatase is expressed in some nucleus of the brain. To assess the functional significance of the aromatase gene in development and activation of sex-specific behavior, we analyzed behavioral phenotypes of the aromatase knockout (ArKO) male mice. ArKO males obviously decreased their fertility and showed deficits in male sexual behavior including mount, intromission and ejaculation. Noncontact penile erection was not significantly affected by defect of the aromatase gene. A reduction of aggressive behavior against male intruders was also observed in ArKO males, while they tend to exhibit aggression toward estrous females during male copulatory tests. Moreover, the infanticide toward the pups was observed in the ArKO males, whereas characteristic parental behavior, but not infanticide was observed in wild-type males. These results indicate that aromatase gene expression is a critical step not only for motivational and consummatory aspects of male sexual behavior, but also for aggressive and parental behaviors in male mice.     

Infanticide among free-ranging langurs (Presbytis entellus) at jodhpur (Rajasthan/India): Recent observations and a reconsideration of hypotheses

Considerable disagreement characterizes the debate concerning frequency, causation, and function of infanticide in connection with adult male replacements in bisexual one-male troops of hanuman langurs (Presbytis entellus). Detailed observations are presented about two noninfanticidal and three infanticidal male changes including six eye-witness and five presumed cases of infanticide within three langur troops during a long-term study at Jodhpur, Rajasthan, India. The results do not support any explanatory hypotheses focussing on social crowding, regulation of population density, social stress, sexual frustration, incest avoidance, or social bonding, but are in general though not total agreement with the reproductive advantage hypothesis: mainly unrelated infants were killed (one possible exception), the infanticidal male generally sired the subsequent offspring (one exception), and the mean interbirth interval subsequent to infanticide is by 2.1 months shortened. Likewise, several cases of stress induced abortions occurred. It is demonstrated that postconception estrous behaviour is by no means a female counterstrategy to infanticide in order to confuse males concerning the issue of paternity, since an infanticidal male did not spare the subsequent offspring of mothers who copulated with him during pregnancy and pregnant females did not discriminate between fathers and non-fathers.     

Changes in Paternal Responsiveness of Prairie Voles (Microtus ochrogaster) in Response to Olfactory Cues and Continuous Physical Contact with a Female

In mammals, paternal care is rarely displayed, and we know little about the mechanisms regulating this behavior. Prairie voles (Microtus ochrogaster) are ideal mammals for the study of paternal behavior because they are a monogamous, bi‐parental species that is easily raised in the laboratory. Paternal responsiveness occurs at moderate levels in sexually‐naive voles and is heightened following a short cohabitation period of 72 h with a female. To determine how increased levels of paternal care are maintained after the initial cohabitation period, we tested the paternal behavior of males that were housed in isolation, were in physical contact with a female, or were exposed to various olfactory cues. The results indicate that the absence of odor cues from a female did not diminish the male’s motivation to care for infants following the initial cohabitation period. In contrast, odor cues from a male appeared to negatively influence the male’s paternal tendencies. The data also show that males that had continuous physical contact with a female spent more time responding paternally and more time hovering over the young compared to males that were housed alone. Together, these results suggest that although paternal behavior is maximized in response to continuous physical contact with females, olfactory cues may not be necessary for the maintenance of heightened paternal behavior.     

Patterns of testosterone and prolactin concentrations and reproductive behavior of helpers and breeders in the cooperatively breeding red-cockaded woodpecker (Picoides borealis)

We examined the proximate causes of delayed breeding and alloparental behavior in the cooperatively breeding red-cockaded woodpecker by measuring plasma concentrations of testosterone (T) and prolactin (PRL) in female breeders, male breeders, and male helpers during different stages of the reproductive cycle. Male breeders and helpers have low T during the prebreeding period, highest T during copulation, and low concentrations of T during the egg-laying/incubation and nestling provisioning stages. Helpers appear physiologically capable of reproducing; their T concentrations equal that of male breeders. Helpers unrelated to the breeding female have higher T than helpers sharing a territory with their mother. Sexual inactivity by male helpers might be explained by behavioral suppression resulting from interactions of male helpers with the breeding pair that somehow differ in accordance with the helper's relatedness to the breeding female (e.g., female breeders are generally unreceptive to courtship from male helpers and least receptive to related helpers). Female breeder, male breeder, and male helper PRL levels did not differ and increased from the prebreeding stage through the copulation and egg-laying/incubation stages. During the nestling provisioning stage, male breeder and helper PRL declined, while female PRL continued to increase. Based on these results, we conclude that the physiological bases of alloparental behavior have not diverged from those that mediate parental behavior in this species.     

Infanticide in male laboratory mice: Effects of social status,prior sexual experience,and basis for discrimination between related and unrelated young

Several aspects of infanticide, including effects of social status, prior sexual experience, and the basis for discrimination between related and unrelated young, were examined in Swiss-Webster laboratory mice (Mus musculus). Strange males introduced into the female's cage for 24 h on day 1 postpartum significantly reduced pup survival whereas the introduction of sires did not. Direct observations of infanticide were frequent, and the motor patterns used by males to kill pups are described. Males killed their own offspring when those young were in the nest of a strange female, whereas most males did not kill unrelated young in the nest of a familiar female. Thus, past association with the mother appears to be the single most important factor mediating male discrimination of young. Prior contact with a specific female's urine reduced a male's propensity for subsequently killing her young. The act of copulation itself also reduced infanticide. Infanticidal behaviour was correlated with the male's social status: most dominant males killed unrelated pups, whereas none of the subordinates engaged in infanticide. These results are discussed in terms of the population biology of this species.     

Is Male Cohabitation Costly for Females of the Spider Stegodyphus lineatus (Eresidae)?

Reproductive interests of females and males can vary over a number of issues, including the number of matings and the occurrence and duration of mate guarding and cohabitation. The mating system of the spider Stegodyphus lineatus (Eresidae) is characterized by an exceptional sexual conflict where males induce females to remate by committing infanticide. Females experience high costs because of this male strategy, while males benefit. During the mating season, males tend to stay with females for several days. We examined whether this male strategy of cohabitation is also disadvantageous for females of S. lineatus. A field experiment revealed that male presence in a female's nest negatively affected her body condition, whereas cohabiting males gained weight because they fed on prey caught in webs of females. As a response, females did not renew their webs when males were present. Thus, females with a cohabiting male experienced the combined cost of prey loss and loss of time available for foraging. These costs are expected to increase with every additional cohabiting male. Mated females behaved more aggressively toward males than did virgin females. This behavior may be interpreted as an adaptive response to reduce mating costs.     

Functional and nonfunctional female receptivity signals in the parasitoid wasp Spalangia endius (Hymenoptera: Pteromalidae)

In many taxa, females signal during courtship when they are receptive. However, just because a female signals does not mean that the male responds to the signal. This study examines female signaling of receptivity (readiness to copulate) and male response in the parasitoid wasp Spalangia endius Walker. Females folded their antennae against their heads when they were receptive, and antennal folding has been shown to be effective in eliciting male copulation attempts in a confamilial. However, male S. endius did not respond to antennal folding: males did not contact the female's antennae during courtship, and how quickly a male attempted copulation was independent of whether or not the female had antennae. Males courted from on top of the female's abdomen and appeared to detect receptivity directly from the female's abdomen rising as her genital orifice opened. On females whose abdomens did not rise, initiation of male copulation attempts were delayed but not eliminated. Based on its current lack of function as a receptivity signal and on comparisons to published reports of mating behavior in confamilials, we hypothesize that female antennal folding at receptivity is a vestigial trait in S. endius.     

Oxytocin and Social Preference in Female House Mice (Mus musculus domesticus)

In social species, same‐sex individuals may form social bonds behaviourally expressed as individual preferences, resulting in fitness benefits such as increased offspring survival, longevity and group cohesion. As a result of individual preferences, female house mice (Mus musculus domesticus) form social affiliations while communally nursing and may do so with kin or non‐kin. However, the mechanisms behind the formation of such preferences are unknown. Oxytocin has been linked to a range of social behaviours including bond facilitation, social memory and parental care. Here, we experimentally increased oxytocin in pairs of unfamiliar, unrelated females and predicted that females with elevated oxytocin would demonstrate increased affiliative behaviours compared against a control. Subsequently, we tested for the formation of a social preference, using a preference test with the previous partner and a new unfamiliar female. Our results indicated no significant effect of treatment on positive and negative behaviours between females during the three initial cohabitation days. In both treatments, females demonstrated increased socio‐positive behaviours and cohabitation time with their partner and decreased socio‐negative behaviours and latency to meet, over the 3‐d period. During the partner preference test, control but not oxytocin females demonstrated a significant preference for their cohabitation partner, and oxytocin females spent similar amounts of time with both stimulus females. Therefore, increasing peripheral oxytocin appears not to be involved in the facilitation of initial encounters with a stranger but may hinder the formation of a preference for this new partner.     

Infanticide and Population Growth in the Bank Vole (Myodes glareolus): The Effect of Male Turnover and Density

One major intrinsic factor affecting recruitment of young into a population is infanticide, the killing of conspecific young by adult males. It occurs in most mammal species, like our study species the bank vole (Myodes glareolus), and is widely accepted as an adaptive behavior, which may increase male fitness via nutritional gain, decreased competition, or an increased access to mates. A turnover of males in a population increases the risk of infanticide owing to a disruption of social structures. In a controlled field study, we tested the effects of total male turnover and density on juvenile recruitment and female space use in experimental bank vole populations. Juvenile recruitment declined significantly in low‐density populations with male turnover, while growth of high‐density populations seemed unaffected. The females’ spatial behavior seemed unaffected by both male turnover and density. Our results suggest that male infanticide may considerably affect population growth and it is more likely to do so at lower densities.     

Comparative paternal and infanticidal behavior of sympatric white-footed mice (Peromyscus leucopus noveboracensis) and deermice (P. maniculatus nubiterrae)

We studied parental and infanticidal behavior in the field andlaboratory in two ecologically equivalent and sympatric congeners,white-footed mice, Peromyscus leucopus noveboracensis, and deermice,P. maniculatus nubiterrae. Despite their close phylogeneticrelationship and ecological similarity, various aspects of parentaland nesting behavior of the two species were significantly different.P. maniculatus males were more paternal than were P. leucopusmales in that they retrieved pups, nested with pregnant femalesand females with newborn pups, and formed longer associationswith females than did P. leucopus males. Thus, P. m. nubiterraeexhibited more pair-bonding (monogamous) characteristics thandid either P. leucopus or P. m. bairdi, as reported in otherstudies. The behavioral differences may represent the differentevolutionary history of the three subspecies. Infanticidal behavior,however, was similar in both species. Dispersing and unmatedmales killed strange pups placed in experimental test chambersin the field, whereas mated males did not kill pups within theirown home ranges. Resident females of both species were moreinfanticidal than were males, killing pups in 90% of the trials.The results support the sexual selection and resource competitionhypotheses for male and female infanticide, respectively. [BehavEcol 1991; 2: 38-45]     

The influence of the parental environment on sexual maturation in male mice

Experiments were designed to examine the influence of either one or both parents on the sexual maturation of male mice. A pregnant female and an adult vasectomized male were housed together and, at delivery, the litter was reduced to 6 pups, 3 of each sex. After weaning, mother, foster-father or both, stayed in cohabitation with their pups until sacrifice. The results showed that: (1) the permanent presence of one or both parents did not affect either testicular growth or the age at first fertile matings. (2) in maturing males (30-40 days), seminal vesicle growth was accelerated by the presence of the mother, inhibited by the presence of the foster-father. (3) in maturing males, the presence of one or both parents lowered plasma testosterone levels. On the opposite, in 90-day-old males, the same conditions increased testosterone levels. These results indicate that only the endocrine function of the testis is affected by the parental environment. The effects are age-dependent.     

Effect of body size and larval experience on mate preference in Helicoverpa armigera (Hübner) (Lep., Noctuidae)

Abstract:  We studied the mating selection in the cotton bollworm, Helicoverpa armigera (Hübner), in relation to body size and larval diet in the laboratory. When provided with an artificial diet at larval stage, weight, body and forewing length did not affect the probability of a male/female moth being selected for mating, but the abdominal width of selected female moths was significantly wider than that of non-selected female moths. 30 female moths were dissected and number of eggs was counted after mating, and there was a correlation between the abdominal width and egg number. There was also significant difference of weight loss between selected and non-selected male/female moths after the mating. The effect of operational sex ratio on mating latency and copulation duration were tested, and the result indicated that mating latency of male selection was significantly longer than that of female selection, but the difference of copulation duration was not significant. Cotton, corn and peanut plants were provided to larvae to test the effect of larval host plant experience on mate choice. When cotton- and peanut-fed moth severed as potential partners, both female and male of cotton-fed moths significantly preferred cotton- to peanut-fed moths for mating. The possible reasons for mate preference based on larval host plant experience may account for host plants attributes on sex pheromone variation and sexual maturity. These findings may impact Bacillus thuringiensis resistance management.     

Distinct preoptic‐BST nuclei dissociate paternal and infanticidal behavior in mice

Paternal behavior is not innate but arises through social experience. After mating and becoming fathers, male mice change their behavior toward pups from infanticide to paternal care. However, the precise brain areas and circuit mechanisms connecting these social behaviors are largely unknown. Here we demonstrated that the c‐Fos expression pattern in the four nuclei of the preoptic‐bed nuclei of stria terminalis (BST) region could robustly discriminate five kinds of previous social behavior of male mice (parenting, infanticide, mating, inter‐male aggression, solitary control). Specifically, neuronal activation in the central part of the medial preoptic area (cMPOA) and rhomboid nucleus of the BST (BSTrh) retroactively detected paternal and infanticidal motivation with more than 95% accuracy. Moreover, cMPOA lesions switched behavior in fathers from paternal to infanticidal, while BSTrh lesions inhibited infanticide in virgin males. The projections from cMPOA to BSTrh were largely GABAergic. Optogenetic or pharmacogenetic activation of cMPOA attenuated infanticide in virgin males. Taken together, this study identifies the preoptic‐BST nuclei underlying social motivations in male mice and reveals unexpected complexity in the circuit connecting these nuclei.     

金色中仓鼠不存在布鲁斯效应

布鲁斯效应是一种由非配偶雄性的化学信号所诱发的雌性妊娠终止现象,曾被认为是雌性对抗雄性杀婴行为的一种进化策略。布鲁斯效应最初在实验小鼠中发现。后续的研究证明了在实验室条件下多种啮齿类动物中存在布鲁斯效应。布鲁斯效应是否为实验室啮齿类动物中存在的普遍规律,目前尚无定论。本实验首先探讨了布鲁斯效应在金色中仓鼠中是否存在。在交配之后给予实验组雌鼠陌生雄鼠的非直接接触刺激,对照组雌鼠接受配偶雄鼠的非直接接触刺激。同时还测定了雌鼠的体重、胚胎质量以及生理器官(肾上腺、脾脏、卵巢和子宫)质量。结果显示,实验组雌鼠的流产率、体重、胚胎质量、生理器官(肾上腺、脾脏、卵巢、子宫)质量与对照组不存在显著差异。本实验结果表明:陌生雄鼠的化学信号对雌性金色中仓鼠的怀孕状态没有影响,实验室条件下的金色中仓鼠不存在布鲁斯效应。     

Fertility in intersubspecific hybrids of laboratory mice (Mus musculus domesticus) and molossinus mice (M. m. molossinus)

We studied the reproductive performance of F1 and F2 hybrids of laboratory mice (C57BL/6, B6 and BALB/c) and molossinus mice (MOM and Mol-A). The F1 x F1 crosses were fully fertile. In the F2 x F2 crosses, the copulation rate was slightly lower and the pregnancy rate was markedly depressed: only 5 out of 18 copulated females (27.8%) became pregnant in the F2 hybrids derived from the reciprocal crosses of B6 x MOM, and in the F2 hybrids from BALB/c x Mol-A crosses, the pregnancy rate was 51.4% (18/35). This low fertility was attributed mainly to the F2 females, because there was a much lower pregnancy rate (56.5%; 26/46) in the (B6 x MOM)F2 female x B6 male crosses compared with the B6 female x (B6 x MOM)F2 male crosses (80.6%; 26/32). On the other hand, the pregnant F2 females were judged to have normal reproductive ability, based on observations of the numbers of corpora lutea, implantations and live fetuses at day 14 of pregnancy. Apparently there is segregation of fertile and sterile females at the F2 generation, but it remains to be determined how the loss of fertility is brought about in the sterile F2 females.