Infanticide risk and infant defence in multi-male free-ranging sooty mangabeys, Cercocebus atys

For years, infanticide by males was thought to be unlikely in multi-male primate species. Recent studies have, however, presented evidence of infanticide in such species and a recent model by Broom and colleagues predicts that males’ age and rank influence the occurrence of infanticide: youngest and highest-ranking immigrant males are more likely to commit infanticide than their older and lower-ranking counterparts if putative fathers fail to protect infants. I collected data on adult free-ranging sooty mangabey females in the Taï National Park, Ivory Coast, over 11 months including a birth and a mating season. Infanticide had been previously reported in captivity for this species, but not in the wild. Several males entered the group prior to and during the mating season. As predicted by the model, only the more dominant immigrant ones attacked mother-infant pairs significantly more often than did other males. Mothers often reacted with counter-attacks. Potential fathers guarded and supported infants and mothers throughout the period of infant vulnerability. Furthermore, as only one of seven infants died despite 136 observed attacks on mother-infant pairs and unattended infants by immigrant males, we conclude that cooperation between putative fathers and mothers represents an effective protection against infanticide.     

Female resistance to invading males increases infanticide in langurs

Background

Infanticide by adult male occurs in many mammalian species under natural conditions, and it is often assumed to be a goal-directed action and explained predominately by sexual selection. Motivation of this behavior in mammals is limitedly involved.

Methodology and Principal Findings

We used long-term reproductive records and direct observation in captivity and in the field of two snub-nosed langur species on the basis of individual identification to investigate how infanticide happened and to be avoided in nonhuman primates. Our observations suggested that infanticide by invading males might be more accidental than goal-directed. The invading male seemed to monopolize all the females including lactating mothers during takeovers. Multiparous mothers who accepted the invading male shortly after takeovers avoided infanticide in most cases. Our results conjectured primiparous mothers would decrease infanticidal possibility if they sexually accepted the invading male during or immediately after takeovers. In the studied langur species, voluntary abortion or mating with the invading male was evidently adopted by females to limit or avoid infanticide by takeover males.

Conclusions and Significance

The objective of the invading male was to monopolize all adult females after his takeover. It appeared that the mother''s resistance to accepting the new male as a mating partner was the primary incentive for infanticide. Motivation analysis might be helpful to further understand why infanticide occurs in primate species.     

Propagation of electromagnetic radiation in mitochondria?

Infanticide by primate males was considered rare if groups contain more than one adult male because, owing to lower paternity certainty, a male should be less likely to benefit from infanticide. Guided by recent evidence for strong variation of infanticide in primate multi-male groups, we modelled the conditions for when infanticide should occur for a group with a resident and an immigrant male. Setting the parameters (e.g. infant mortality, reduction of interbirth interval, life-time reproductive success, genetic representation) to fit the conditions most commonly found in nature, we develop a game-theoretic model to explore the influence of age and dominance on the occurrence of infanticide and infant defence. Male age strongly impacts the likelihood of an attack which is modified by the father's defence. If the new male is dominant he is likely to attack under most circumstances whereas a subordinate male will only attack if the father does not defend. These model scenarios fit the conditions under which infanticide is known to occur in primate multi-male groups and offer an explanation why infanticide is common in some multi-male groups and rare in others. Overall, the benefits for infanticidal males are strongly governed by a reduced interbirth interval while advantages via improved genetic representation in the gene pool contribute but a minor fraction.     

The evolution of non-maternal care in anthropoid primates: a test of the hypotheses

The amount of non-maternal care (allocare) found in primates varies greatly from species to species. Our paper examines this variation and focuses on possible reasons why mothers in some anthropoid primate species are prepared to relinquish their infants to other carers whereas others are not. We use data collected from the literature to test a number of hypotheses that attempt to explain the observed variation in non-maternal care. Analyses were carried out using comparative methods that control for the influence of both body size and phylogeny on life-history and ecological variation. The results support previous studies of both primates and other mammals in finding a clear link between the amount of allocare provided and female reproductive rates. Species with high allocare levels grow rapidly post-natally and wean their infants at a younger age (but at the same relative size) than species of the same body size with lower allocare levels. This early weaning allows high allocare species to support higher birth rates than low allocare species but does not result in earlier maturation. Our results, therefore, suggest that mothers allow non-maternal care of their infants in order to increase their own reproductive output. It is not clear whether such a strategy also benefits the infant, as we could find no link between the presence of allocare and early maturation (which would increase the infant's reproductive output) or between allocare levels and infant survival (as measured by vulnerability to infanticide). This suggests that mothers and infants might come into conflict over transfer to other carers, as the benefits to the mother may not be accompanied by benefits to the infant. However, although mothers may benefit from allocare in some circumstances, they will not be expected to allow allocare if the costs are high (e.g. if there is a high risk to the infant).     

Infanticide in primates and man and the problems of reconstructing the social behavior of the hominids

The general analysis of infanticide distribution pattern in primate and human populations is given. The possibilities to use the sociobiological, ecological, psycho-analytical and structural-social approaches are considered to explain the infanticide functions in primates. The necessity of exact data concerning the sex, age and social position of both: killers and victims (victim's mothers either) is stressed, as well the estimation of social situation in the group in the period before the infanticide. The qualitative differences in infanticide mechanisms in lower monkeys, anthropoids and man is illustrated. It is proposed to differentiate the infanticide on the individual level and as a group social strategy. The probability of infanticide in hominid societies on the different stages of evolution is discussed.     

Victims of Infanticide and Conspecific Bite Wounding in a Female-Dominant Primate: A Long-Term Study

The aggression animals receive from conspecifics varies between individuals across their lifetime. As poignantly evidenced by infanticide, for example, aggression can have dramatic fitness consequences. Nevertheless, we understand little about the sources of variation in received aggression, particularly in females. Using a female-dominant species renowned for aggressivity in both sexes, we tested for potential social, demographic, and genetic patterns in the frequency with which animals were wounded by conspecifics. Our study included 243 captive, ring-tailed lemurs (Lemur catta), followed from infancy to adulthood over a 35-year time span. We extracted injury, social, and life-history information from colony records and calculated neutral heterozygosity for a subset of animals, as an estimate of genetic diversity. Focusing on victims rather than aggressors, we used General Linear Models to explain bite-wound patterns at different life stages. In infancy, maternal age best predicted wounds received, as infants born to young mothers were the most frequent infanticide victims. In adulthood, sex best predicted wounds received, as males were three times more likely than females to be seriously injured. No relation emerged between wounds received and the other variables studied. Beyond the generally expected costs of adult male intrasexual aggression, we suggest possible additive costs associated with female-dominant societies – those suffered by young mothers engaged in aggressive disputes and those suffered by adult males aggressively targeted by both sexes. We propose that infanticide in lemurs may be a costly by-product of aggressively mediated, female social dominance. Accordingly, the benefits of female behavioral ‘masculinization’ accrued to females through priority of access to resources, may be partially offset by early costs in reproductive success. Understanding the factors that influence lifetime patterns of conspecific wounding is critical to evaluating the fitness costs associated with social living; however, these costs may vary substantially between societies.     

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

Infanticide 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.     

Mating strategies in primates: a game theoretical approach to infanticide

Infanticide by newly immigrated or newly dominant males is reported among a variety of taxa, such as birds, rodents, carnivores and primates. Here we present a game theoretical model to explain the presence and prevalence of infanticide in primate groups. We have formulated a three-player game involving two males and one female and show that the strategies of infanticide on the males' part and polyandrous mating on the females' part emerge as Nash equilibria that are stable under certain conditions. Moreover, we have identified all the Nash equilibria of the game and arranged them in a novel hierarchical scheme. Only in the subspace spanned by the males are the Nash equilibria found to be strict, and hence evolutionarily stable. We have therefore proposed a selection mechanism informed by adaptive dynamics to permit the females to transition to, and remain in, optimal equilibria after successive generations. Our model concludes that polyandrous mating by females is an optimal strategy for the females that minimizes infanticide and that infanticide confers advantage to the males only in certain regions of parameter space. We have shown that infanticide occurs during turbulent changes accompanying male immigration into the group. For changes in the dominance hierarchy within the group, we have shown that infanticide occurs only in primate groups where the chance for the killer to sire the next infant is high. These conclusions are confirmed by observations in the wild. This model thus has enabled us to pinpoint the fundamental processes behind the reproductive decisions of the players involved, which was not possible using earlier theoretical studies.     

Infanticide in the evolution of reproductive synchrony: effects on reproductive success

Synchronous breeding in animals and plants has stimulated both a theoretical and empirical examination of the possible benefits of active synchronization. The selective pressures of predation and infanticide are the strongest candidates proposed to explain the evolution of reproductive synchrony. Alternatively, breeding asynchronously with conspecifics may ensure a greater availability of resources per breeder. However, the possible fitness benefits resulting from active asynchronization have not yet received attention in evolutionary ecology. Here we present a hypothesis, based on a graphical model, illustrating the costs and benefits of the two modes of reproduction. We tested the hypothesis empirically using a 2 x 2 full factorial study design, where reproductive synchrony and infanticide tactics were manipulated in enclosed populations of the bank vole. The results reveal a relationship between infanticide tactics and breeding synchrony as illustrated by our hypothesis. In general, female reproductive success (number and size of offspring surviving to weaning) was significantly lower in infanticidal populations. Moreover, an asynchronous breeding pattern proved to be advantageous in the noninfanticidal population but this advantage of asynchrony was lost as infanticide became common in the population. Our findings support the idea that synchronous reproduction could have evolved as a counterstrategy against infanticide.     

The role of survival for the evolution of female philopatry in a solitary forager, the grey mouse lemur (Microcebus murinus)

It is widely accepted that natal philopatry is a prerequisite for the evolution of sociality. The life-history hypothesis maintains that longevity of adults results in extended territory tenure and thus limits breeding vacancies for offspring, which makes natal philopatry more likely. Here, we tested the importance of longevity for natal philopatry in females of a basal primate, the grey mouse lemur (Microcebus murinus). This species is regarded as being solitary due to its foraging habits but while males disperse, female offspring in this species forgo dispersal and form long-term sleeping groups with their mothers. We tested whether high adult survival could be a cause for natal philopatry of female offspring. In addition, we assessed costs and benefits associated with space sharing between mothers and daughters and whether mothers actively increase survival of daughters by beqeauthal of territories, information transfer about resources or thermoregulation. Contrary to our predictions, adult females had low-survival rates. Space sharing appeared to improve survival of both, mothers and daughters. This could be a result of information transfer about sleeping sites and thermoregulatory benefits. Our results cast doubt on the idea that longevity predisposes species for social traits and provide support for benefits of philopatry.     

The evolution of male infanticide in relation to sexual selection in mammalian carnivores

The evolution of infanticide by males has often been explained by the sexual selection hypothesis, which posits that infanticide improves male reproductive success by shortening the interbirth intervals of the mothers of the killed offspring. In Carnivora, however, the fitness advantages assumed in this hypothesis have been shown in only a few species, and it has been argued that male infanticide may be nonadaptive in pinniped carnivores. According to the sexual selection hypothesis, male infanticide is expected to be more prevalent in species in which males are subjected to stronger sexual selection through intrasexual competition over mates. We examined a phylogenetically corrected relationship between male infanticide and sexual size dimorphism (SSD) as a measure of the intensity of sexual selection in carnivores. Our analyses failed to detect a significant association between the occurrence of male infanticide and SSD across carnivores, although they showed that, among fissipeds (typically terrestrial carnivores), males in species with stronger male-biased SSD are significantly more likely to commit infanticide. This suggests that the evolution of male infanticide is correlated with intense sexual selection in fissipeds. In pinnipeds (Odobenidae, Otariidae, and Phocidae), there was no significant association between male infanticide and SSD. Assuming that SSD represents the intensity of sexual selection on males, this result is consistent with the argument that infanticide by male pinnipeds is not a sexually selected behaviour.     

Proximity patterns of female western lowland gorillas (Gorilla gorilla gorilla) during the six months after parturition

Studies of wild mountain gorillas have demonstrated strong preferences among new mothers for the silverback. Protection against infanticide has been theorized to be the primary cause for this attraction. We examined social partner preferences in captive western lowland mothers during the 6 mo after parturition and found that juveniles and females were the primary members of the new mothers' social network. Mothers spent significantly more time in close proximity with both of these subgroups than with the silverback. Proximity patterns changed over time: new mothers spent more time near females in the month after parturition than in the month prior to parturition, and spatial proximity increased again in months 2-6 postparturition. These findings differ from those reported for wild mountain gorillas, which may reflect the lack of infanticide risk in captivity. Given current hypotheses that infanticide may be a limited in western lowland gorillas, the social partner preferences observed here may be indicative of patterns in wild populations.     

Cross-generational fitness effects of infection in Drosophila melanogaster

Activation of the immune system is beneficial in defending against pathogens, but may also have costly side effects on an organism's fitness. In this study we examine the fitness consequences of immune challenge in female Drosophila melanogaster by examining both direct (within generation) and indirect (between generations) costs and benefits of immune challenge. Though passing immunity to offspring has been studied in mammals for many years, only recently have researchers found evidence for a cross-generational priming response in invertebrates. By examining both potential fitness costs and benefits in the next generation, we were able to determine what effect immune challenge has on fitness. In agreement with other studies, we found a direct cost to infection, where immune challenged females laid fewer eggs than unchallenged females in two of the three lines we examined. In addition, we found some evidence for indirect costs. Offspring from immune challenged mothers had shorter lifespans than those from unchallenged mothers in two of the three lines. Interestingly, we do not see any effect of maternal immune challenge on offspring's ability to overcome an infection, nor do we see an effect on other fitness traits measured, including egg size, egg-adult viability, and offspring resistance to oxidative stress. While previous studies in bumblebees and beetles have demonstrated cross-generation priming, our results suggest that it may not be a general phenomenon, and more work is needed to determine how widespread it is.     

Why do chimpanzee males attack the females of neighboring communities?

Our closest nonhuman primate relatives, chimpanzees, engage in potentially lethal between‐group conflict; this collective aggressive behavior shows parallels with human warfare. In some communities, chimpanzee males also severely attack and even kill females of the neighboring groups. This is surprising given their system of resource defense polygyny, where males are expected to acquire potential mates. We develop a simple mathematical model based on reproductive skew among primate males to solve this puzzle. The model predicts that it is advantageous for high‐ranking males but not for low‐ranking males to attack females. It also predicts that more males gain a benefit from attacking females as the community's reproductive skew decreases, i.e., as mating success is more evenly distributed. Thus, fatal attacks on females should be concentrated in communities with low reproductive skew. These attacks should also concur with between‐community infanticide. A review of the chimpanzee literature provides enough preliminary support for this prediction to warrant more detailed testing. Am J Phys Anthropol 155:430–435, 2014. © 2014 Wiley Periodicals, Inc.     

New records of within-group infanticide and cannibalism in wild chimpanzees

Two cases of within-group infanticide and cannibalism were observed among the M Group chimpanzees of the Mahale Mountains, Tanzania. In both cases, victimized infants were male, 5 – 6 months of age, and in good health when killed. Four to five years have passed since the mothers of the victims immigrated into M Group as nulliparous immigrants. In one case the 2nd-ranking male was observed to detach the infant from the mother's belly. Both infants were finally killed by the alpha male after several adult males scrambled for the bodies. There was no evidence that the mothers had mated with males other than those of M Group. Nor was there evidence that the mothers had restrictive mating relationships with some of the M Group adult males. What little evidence is available shows that the mothers had mated mostly with adolescent and other immature males during their conception cycles. However, at least in one case, the mother began to mate more with adult males rather than with immature males after the infanticide. It is proposed that the function of within-group male infanticide can be explained by the male-male competition hypothesis developed for hanuman langurs and other nonhuman primates.     

非人灵长类是否回避近亲繁殖?

近亲繁殖回避现象是人类学者、生物学者、心理学者和社会学者最关心的研究课题之一。针对灵长类的社会特点和近亲繁殖回避假说,本文引入了三个主要假设:假设1)近亲繁殖可能会导致个体繁殖适合度降低等损失;假设2)近亲繁殖有利有弊,但是弊端可能明显大于利益;假设3)如果弊大于利,那么动物应该进化形成回避近亲繁殖的机制,以减少该行为产生的损失。然后,本文综述分析了6科19个灵长类种群的现有繁殖数据,验证了灵长类的行为回避、迁移和繁殖抑制等机制,旨在强调灵长类回避近亲繁殖的必要性及其生物学背景,并为人类学、生物学和心理学的相关研究提供跨学科素材。     

Impact of Male Infanticide on the Social Structure of Mountain Gorillas

Infanticide can be a major influence upon the social structure of species in which females maintain long-term associations with males. Previous studies have suggested that female mountain gorillas benefit from residing in multimale groups because infanticide occurs when one-male groups disintegrate after the dominant male dies. Here we measure the impact of infanticide on the reproductive success of female mountain gorillas, and we examine whether their dispersal patterns reflect a strategy to avoid infanticide. Using more than 40 years of data from up to 70% of the entire population, we found that only 1.7% of the infants that were born in the study had died from infanticide during group disintegrations. The rarity of such infanticide mainly reflects a low mortality rate of dominant males in one-male groups, and it does not dispel previous observations that infanticide occurs during group disintegrations. After including infanticide from causes other than group disintegrations, infanticide victims represented up to 5.5% of the offspring born during the study, and they accounted for up to 21% of infant mortality. The overall rates of infanticide were 2–3 times higher in one-male groups than multimale groups, but those differences were not statistically significant. Infant mortality, the length of interbirth intervals, and the age of first reproduction were not significantly different between one-male versus multimale groups, so we found no significant fitness benefits for females to prefer multimale groups. In addition, we found limited evidence that female dispersal patterns reflect a preference for multimale groups. If the strength of selection is modest for females to avoid group disintegrations, than any preference for multimale groups may be slow to evolve. Alternatively, variability in male strength might give some one-male groups a lower infanticide risk than some multimale groups, which could explain why both types of groups remain common.     

Promiscuous females protect their offspring

Multi-male mating (MMM) by females is relatively common among mammals, occurring in at least 133 species and several evolutionary benefits of MMM have been proposed. The most convincing explanation is that MMM confuses paternity, thereby deterring infanticide by males. A second explanation for females that are unlikely to experience infanticide is that MMM is a consequence of sexual harassment. Mate guarding and, perhaps even in some cases, behavioral monogamy, might have evolved in response to the threat of infanticide and the subsequent tendency for females to mate multiply. Benefits relating to improved genetic fitness of offspring do occur in some species, but do not provide a widespread explanation for the evolutionary origin of MMM; if cryptic female choice through sperm competition is adaptive to females it probably evolved as a consequence of, rather than a precursor to, female promiscuity. Here, we provide support for the original hypothesis of paternity confusion for MMM, rather than for the more popular good genes or sperm competition hypotheses.     

Infant Mortality Risk and Paternity Certainty Are Associated with Postnatal Maternal Behavior toward Adult Male Mountain Gorillas (Gorilla beringei beringei)

Sexually selected infanticide is an important source of infant mortality in many mammalian species. In species with long-term male-female associations, females may benefit from male protection against infanticidal outsiders. We tested whether mountain gorilla (Gorilla beringei beringei) mothers in single and multi-male groups monitored by the Dian Fossey Gorilla Fund’s Karisoke Research Center actively facilitated interactions between their infants and a potentially protective male. We also evaluated the criteria mothers in multi-male groups used to choose a preferred male social partner. In single male groups, where infanticide risk and paternity certainty are high, females with infants <1 year old spent more time near and affiliated more with males than females without young infants. In multi-male groups, where infanticide rates and paternity certainty are lower, mothers with new infants exhibited few behavioral changes toward males. The sole notable change was that females with young infants proportionally increased their time near males they previously spent little time near when compared to males they had previously preferred, perhaps to encourage paternity uncertainty and deter aggression. Rank was a much better predictor of females’ social partner choice than paternity. Older infants (2–3 years) in multi-male groups mirrored their mothers’ preferences for individual male social partners; 89% spent the most time in close proximity to the male their mother had spent the most time near when they were <1 year old. Observed discrepancies between female behavior in single and multi-male groups likely reflect different levels of postpartum intersexual conflict; in groups where paternity certainty and infanticide risk are both high, male-female interests align and females behave accordingly. This highlights the importance of considering individual and group-level variation when evaluating intersexual conflict across the reproductive cycle.     

A theory of gene-culture coevolution of parental preference and sex ratio in humans

A theory on the evolution of human primary sex ratio is proposed. Effects of parental preference for sons, reflected in birth control based on offspring sex ratio and female biased infanticide, on the evolution of primary sex ratio are analyzed. Both are shown to select for female bias in primary sex ratio. The gene-culture coevolution of female infanticide and primary sex ratio is also studied and it is shown that female infanticide develops more in societies in which the father plays a more important role in the transmission of culture than the mother does.