Infanticide in Propithecus diadema edwardsi: An Evaluation of the Sexual Selection Hypothesis

Infanticide might be described as a reproductive strategy employed by anthropoid primate males when they immigrate into new groups. But infanticide has rarely been observed in wild prosimian primates. For the Malagasy lemurs this may reflect one or more of the following: strict breeding seasons; relative monomorphism in canine tooth and body size; small group sizes; male–female dominance relations; and male–female dyads within groups. We addressed the following questions: Do prosimian males commit infanticide in circumstances similar to those in which anthropoids do? and Is there any reproductive advantage for a highly seasonal breeder to commit infanticide? To help answer these questions, we describe the death of a 24-hr-old infant male Propithecus diadema edwardsi from wounds received during a fight between his mother, her adult daughter, and a newly immigrant male. Interbirth intervals between surviving offspring are 2 years for Propithecus diadema edwardsi; therefore, a male could dramatically shorten the time between reproductive windows by killing an infant. Whether this tactic would be favored by sexual selection cannot be addressed until more information has been collected on the length of interbirth interval due to infanticide relative to that of infant death by other causes; how social factors such as stability of breeding relationships affect long-term male reproductive success; how effective female counterstrategies are to prevent infanticide and/or whether they choose to mate with males that commit infanticide; and how often males that kill infants subsequently sire infants, particularly in groups that contain a resident male.     

Male Infanticide in the Golden Snub-Nosed Monkey (<Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis>), a Seasonally Breeding Primate

In nonhuman primates, infanticide by adult males can occur when the leader male is ousted from a one-male, multifemale group, or when male dominance rank changes within a multimale, multifemale group. According to the sexual selection hypothesis, this behavior may be adaptive if perpetrators increase their reproductive success by killing unrelated, unweaned infants, thus shortening the interbirth interval of the mother, and then siring her next infant. Under an alternative hypothesis, infanticide is a byproduct of aggressive male–male competition and these predictions do not hold. Direct observations of the context surrounding infanticide in free-ranging primate populations that allow a test of these predictions are rare. Here, we document four cases of male infanticide and report paternity data for a group of golden snub-nosed monkeys (Rhinopithecus roxellana) at Shennongjia, China. Three cases of infanticide by new leader males supported the predictions of the sexual selection hypothesis, while another provides partial support for the sexual selection hypothesis, but can also be explained via a nonadaptive hypothesis. In this latter case, a male from an all-male group killed an infant during an aggressive episode that appeared to be accidental, as it took place 7 mo before a male takeover happened, and the perpetrator did not obtain any reproductive advantage. We conclude that most male infanticide events in golden snub-nosed monkeys are consistent with the adaptive selection sexual hypothesis.     

Potentially infanticidal behavior in the Amazon river dolphin (<Emphasis Type="Italic">Inia geoffrensis</Emphasis>)

Infanticide by males is a phenomenon common in species in which the reproductive output of large numbers of females can be monopolized by a small number of males. It is thought to increase a male’s fitness, at the expense of the fitness of the infant’s parents, by bringing females into season more quickly. Infanticide by males has been recorded in just three cetacean species. We report aggressive behavior suggestive of infanticide in a fourth, the Amazon river dolphin (Inia geoffrensis). We observed and photographed a series of attacks on a neonate Amazon river dolphin by a large male, with apparent protective behavior by the mother. Although infanticide was not confirmed, the forceful, aggressive behaviors were highly suggestive of infanticidal behavior and represent another important data point for comparative studies of infanticide in mammals. Amazon river dolphins may have a polygynous, polyandrous, or promiscuous mating system, the latter two of which are not the norm in species in which the reproductive output of large numbers of females are monopolized by a small number of males. However, sexual dimorphism, high rates of aggression by males, socio-sexual object-carrying displays by males, and a long interbirth interval suggest that successful male Amazon river dolphins may be able to monopolize a large proportion of mating opportunities, and it is plausible that male dolphins can improve their reproductive success by bringing females into estrous sooner by killing the offspring of other males.     

Infant loss during and after male replacement in gibbons

According to the sexual selection hypothesis, infanticide during resident male replacement is an adaptive strategy that has evolved because the killing of unweaned offspring sired by previous males shortens the inter‐birth intervals of the mothers whose infants are targeted and thereby increases the reproductive fitness of the perpetrator. To test this hypothesis, we describe previously unreported cases of primary male replacement for two gibbon species (Hylobates lar and Nomascus nasutus), and review all other reported cases of primary male replacement in gibbons. Overall, infants were present in nearly half of all cases (16/33, 48%) and of the 18 infants present during replacement, 50% (N = 9) disappeared within 2 months of the event. In four of the five cases where there was sufficient demographic information to identify the likely sire of the subsequent offspring of females that lost infants, the new male was believed to be the sire. Infants were also less likely to die or disappear if the new male and original resident male were possible kin. However, there was no significant difference in the age of infants between those that died or disappeared following replacement and those that survived to weaning (p = .630). Our review of takeover‐related infant loss in gibbons confirms that periods of male instability are risky for unweaned infants and that replacing males benefit from infant loss. Nevertheless, variability in the context of infant loss and difficulties related to data collection in the field make it difficult to test competing hypotheses concerning the mechanisms and functions of infanticide in the small apes.     

Male Demography,Female Mating Behavior,and Infanticide in Wild Patas Monkeys (Erythrocebus patas)

Infanticide by males has been hypothesized to be a naturally selected behavioral strategy that increases the infanticidal male's reproductive success. The sexual selection hypothesis has been challenged via alternative, nonadaptive hypotheses that dispute its empirical and theoretical bases. Two of the most widely recognized alternatives are the social pathology hypothesis, in which infanticide results from overcrowding or recent human disturbance, and the generalized aggression hypothesis, in which infanticide is an epiphenomenon of increased male aggression. We report the first case of infanticide in wild, seasonally breeding patas monkeys (Erythrocebus patas) living at a low population density in a stable habitat, conditions which do not support the social pathology hypothesis. Its exceptional occurrence is consistent with the sexual selection hypothesis: over a 7-year period the infanticidal male was the only one of 13 resident males that was not present during the actual conception season but was present during the following birth season. Also consistent with this hypothesis, mothers were differentially targeted for male aggression, which increased sevenfold during the days surrounding the infanticide and then decreased to baseline levels after the infanticide. Aggression targeted at mothers does not support the generalized aggression hypothesis. As predicted by the sexual selection hypothesis, females began soliciting mating immediately after the infanticide, despite its occurrence in the nonconceptive season.     

Concealed fertility and extended female sexuality in a non-human primate (Macaca assamensis)

In numerous primates living in mixed-sex groups, females display probabilistic cues of fertility to simultaneously concentrate paternity to dominant males while diluting it amongst others as a means to reduce the risk of infanticide and to increase male care for offspring. A few species, however, lack these cues and potentially conceal fertility from males; yet, to date, little is known about mating patterns and their underlying proximate mechanisms in such species. Here, we investigated mating activity and sexual consortships relative to female reproductive state in wild Assamese macaques (Macaca assamensis), a species where females lack prominent anogenital swellings and copulation calls. During two mating seasons (2837 contact hours) we recorded sexual and social behaviors, sexual consortships, and collected 1178 fecal samples (n = 15 females) which were analyzed for progestogen concentrations to assess female reproductive state and to determine the timing of ovulation and conception. Although mostly conceiving in their first ovarian cycle, females were sexually receptive throughout the entire 4-month mating season, and within-cycle mating frequencies were not increased during fertile phases. Dominant males did not monopolize fertile matings, and consortships by high-ranking males lasted for long periods, which were not exclusively linked to female fertile phases. Furthermore, females copulated promiscuously but not randomly, i.e. for almost every female, matings were concentrated to a certain male, irrespective of male rank. Collectively, we demonstrate that fertility is undisclosed to males. The extreme extended female sexuality facilitated by concealed fertility may allow females to create differentiated mating relationships within a promiscuous mating system. Our study provides important new insight into the plasticity of female sexuality in non-human primates.     

A case of infanticide in a recently found gelada population in Arsi, Ethiopia

There have been no reports of infanticide in wild gelada baboons and it has been argued that infanticide is not necessary in geladas, since the birth interval of female gelada can be shortened after takeover of a unit by a new leader male without infanticide. However, we observed an instance of infanticide in a newly-found wild gelada population in the Arsi Region of Ethiopia. After a leader male of the unit was severely wounded by a leopard attack, he was quite weakened. The second male of the unit, a young adult male, became the leader of the unit three weeks later, but the former leader continued to stay in the unit as a second male. After a week, two other adult males joined the unit which, therefore, came to include four adult males. The infanticide took place nine days later. The perpetrator was one of the immigrant males and he showed great interest in the mother of the unweaned victim infant. Although the perpetrator copulated with her after the infanticide, the usurper was found to own all three adult females after two weeks following the infanticide; i.e. the perpetrator could not own any female. The wounded former leader showed conspicuous protective behavior towards the victim's mother and the dead infant. One possible explanation for the occurrence of infanticide in this population of geladas is as follows. Gelada males in this area may be able to join units more easily to form multi-male units but then have shorter tenure in the units. Facing the unstable condition of units, they may sometimes engage in infanticide to increase their breeding opportunities, even before becoming a leader.     

DNA analyses support the hypothesis that infanticide is adaptive in langur monkeys.

Although the killing of dependent infants by adult males is a widespread phenomenon among primates, its causes and consequences still remain hotly debated. According to the sexual selection hypothesis, infanticidal males will gain a reproductive advantage provided that only unrelated infants are killed and that the males increase their chances of siring the next infants. Alternatively, the social pathology hypothesis interprets infanticide as a result of crowded living conditions and, thus, as not providing any advantage. Based on DNA analyses of wild Hanuman langurs (Presbytis entellus) we present the first evidence that male attackers were not related to their infant victims. Furthermore, in all cases the presumed killers were the likely fathers of the subsequent infants. Our data, therefore, strongly support the sexual selection hypothesis interpreting infanticide as an evolved, adaptive male reproductive tactic.     

Sexually selected infanticide in a polygynous bat

Background

Adult individuals of many species kill unrelated conspecific infants for several adaptive reasons ranging from predation or resource competition to the prevention of misdirected parental care. Moreover, infanticide can increase the reproductive success of the aggressor by killing the offspring of competitors and thereafter mating with the victimized females. This sexually selected infanticide predominantly occurs in polygynous species, with convincing evidence for primates, carnivores, equids, and rodents. Evidence for bats was predicted but lacking.

Methodology/Principal Findings

Here we report the first case, to our knowledge, of sexually selected infanticide in a bat, the polygynous white-throated round-eared bat, Lophostoma silvicolum. Behavioral studies in a free-living population revealed that an adult male repeatedly attacked and injured the pups of two females belonging to his harem, ultimately causing the death of one pup. The infanticidal male subsequently mated with the mother of the victimized pup and this copulation occurred earlier than any other in his harem.

Conclusions/Significance

Our findings indicate that sexually selected infanticide is more widespread than previously thought, adding bats as a new taxon performing this strategy. Future work on other bats, especially polygynous species in the tropics, has great potential to investigate the selective pressures influencing the evolution of sexually selected infanticide and to study how infanticide impacts reproductive strategies and social structures of different species.     

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.     

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.     

Sexual selection in the monogamous barn swallow (Hirundo rustica). II. Mechanisms of sexual selection

Mechanisms of sexual selection in the monogamous, sexually dimorphic barn swallow (Hirundo rustica) were studied during a seven-year period. First, the sex ratio of reproducing adults was male-biased, and mated males had significantly longer tail ornaments than unmated males. Secondly, some of the unmated individuals later committed infanticide and became mated with the mother of the killed brood. Fathers of killed broods had significantly shorter tails than other males, and there was a tendency for infanticidal males to have longer tail ornaments than other unmated males. Thirdly, long-tailed male barn swallows were more successful in acquiring extra-pair copulations than other males, and females involved in extra-pair copulations, as compared to females not involved in such copulations, had mates with shorter tail ornaments. Fourthly, male barn swallows having long tails as compared to short-tailed males acquired mates in better body condition. Females mated to long-tailed males reproduced earlier, laid more eggs and were more likely to have two clutches than were females mated to short-tailed males. Finally, females mated to long-tailed males put more effort into reproduction than did other females, as evidenced by their relatively larger contribution to feeding of offspring. Thus, at least five different components of sexual selection affected male reproductive success. Selection arising from differential success during extra-pair copulations, differential reproductive success and differential male reproductive effort thus accounted for most of the selection on tail ornaments in male barn swallows.     

Infanticide and juvenilicide in Hanuman langurs (Presbytis entellus) around Jodhpur,India

Ten cases of infant killings and 2 cases of juvenile killings were observed in two troops of Hanuman langurs, (Presbytis entellus) around Jodhpur, India. Fatal attacks on infants and juveniles are classified into four categories. The process of infanticide was observed from start to end and is described in detail for 3 cases. The age of the victims ranged from 0.2 to 48 months. The interbirth interval among females whose infants were killed is significantly shorter compared to females whose infants survived. In ourt study, 7 cases support the reproductive advantage hypothesis, that infanticide is an adaptive behaviour to increase male reproductive success. The remaining 5 cases do not fit into the reproductive advantage hypothesis. In these cases, victims are over 8 months old, and as such their deaths could not shorten the interbirth interval. It appears that by killing older infants and juveniles the males obtain an advantage in resource competition for their offspring. An alternative is that new males chase or peripheralise the older infants and juveniles, which leads to 97% predominant uni-male troop structure in Jodhpur.     

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.     

Male‐mediated prenatal loss: Functions and mechanisms

Sexually selected infanticide has been the subject of intense empirical and theoretical study for decades; a related phenomenon, male‐mediated prenatal loss, has received much less attention in evolutionary studies. Male‐mediated prenatal loss occurs when inseminated or pregnant females terminate reproductive effort following exposure to a nonsire male, either through implantation failure or pregnancy termination. Male‐mediated prenatal loss encompasses two sub‐phenomena: sexually selected feticide and the Bruce effect. In this review, we provide a framework that explains the relationship between feticide and the Bruce effect and describes what is known about the proximate and ultimate mechanisms involved in each. Using a simple model, we demonstrate that male‐mediated prenatal loss can provide greater reproductive benefits to males than infanticide. We therefore suggest that, compared to infanticide, male‐mediated prenatal loss may be more prevalent in mammalian species and may have played a greater role in their social evolution than has previously been documented.     

Sexual swellings in female hamadryas baboons after male take-overs: "deceptive" swellings as a possible female counter-strategy against infanticide

In many primate species, male intanticide is assumed to pose a serious risk for infants, and therefore female counter-strategies are expected. These counter-strategies may include changes in the females' reproductive behavior and physiology, e.g., mating with multiple males and prolonged receptivity. Since the risk of infanticide is particularly high when a new male enters the group or when a male rises in rank, we studied the changes in female reproductive conditions, e.g., post-partum amenorrhea and interbirth intervals, following group take-overs by new males in a captive group of hamadryas baboons (Papio h. hamadryas). Following take-overs, five out of six lactating females immediately developed sexual swellings, thus shortening their post-partum amenorrhea. However, none of these females conceived during the first cycles after the take-over, their reproduction was not accelerated, and four out of five dependent infants survived. Thus, interbirth intervals did not decrease compared to times with no group take-overs. We therefore suggest that these situation-dependent swellings are used by female hamadryas baboons as a counter-strategy to reduce the risk of infanticide, which exists in this species after male take-overs. By offering new males mating opportunities without allowing them to reproduce, females may increase their infants' probability of survival and at the same time avoid the costs of being pregnant and lactating simultaneously.     

New Case of Intragroup Infanticide in the Chimpanzees of Gombe National Park

Researchers have reported a total of 31 infanticides in 4 different chimpanzee (Pan troglodytes) populations. Though infanticide is infrequent, low reproductive rates of females likely make it a strong selective pressure in the species. We report a new incident of intragroup infanticide in Gombe National Park, Tanzania, in which a community male attacked a 3.5-yr-old male. We then consider the infanticide in terms of adaptive and nonadaptive explanations for infanticide including the social pathology, by-product of male aggression, nutritive benefits, resource competition, and sexual selection hypotheses. The incident reported here is not well explained by any of them. While the infanticide is puzzling in terms of ultimate explanations for infanticide, it provides a good context in which to consider proximate mechanisms for offspring recognition. The incident provides some evidence that males may use their mating history with the mother to assess paternity likelihood.     

Infanticide in black capuchin monkeys (Cebus apella nigritus) in Iguazú National Park, Argentina

We report here one observed and two potential cases of infanticide during a brief period of 1 month after a dominant male replacement in one group of black capuchin monkeys in Iguazú National Park, Argentina. We also compile infant disappearances and demographic data in seven groups followed from 1-14 years. Behavioral and molecular data showed that the probability that an infanticidal male would kill his own progeny is very low in this species. Females that lost infants less than 6 months old had shorter interbirth intervals than females whose infants survived (14.12 ± 5.32 months, n=17 vs. 20.42 ± 5.65 months, n=34). Females whose infants die shortly after takeovers mate with the presumed infanticidal male during the most fertile days of their subsequent estrous periods giving this male a high probability of siring the new progeny. We recorded 181 proceptive periods and 52 births from 18 adult females in two groups. Most proceptive periods were concentrated during a conception season, but there was an increase in sexual behavior after male takeovers. Seven females copulated while pregnant after the observed male takeover, an unusual behavior in this species in years of group stability. Of 24 infants born during takeover years, 62.5% did not survive the first year, whereas only 22.5% of 80 infants died in years without male replacements. We found a significant positive association between infant mortality and male takeovers, but not with food provisioning. The main cause of infant mortality in this population is associated with male takeovers. Our results suggest that infanticide can have an important effect on the behavior of this species, selecting for female behaviors that function to reduce infanticide risk.     

New cases of inter-community infanticide by male chimpanzees at Ngogo,Kibale National Park,Uganda

Infanticide by males has been recorded in four chimpanzee populations, including that in Kibale National Park, Uganda. Some infanticidal attacks occur during inter-community aggression. The sexual selection hypothesis does not easily explain these attacks because they may not directly increase male mating opportunities. However, females in the attackers’ community may benefit by expanding their foraging ranges and thereby improving their reproductive success; thus infanticide may increase male reproductive success indirectly. We report two new cases of infanticide by male chimpanzees at Ngogo, Kibale National Park. Like two previous cases, these occurred during a boundary patrol and were almost certainly between-community infanticides. The patrolling males attacked despite the proximity of males from the victims’ presumed community. This probably explains why, unlike the earlier cases, they did not completely cannibalize their victims. Such attacks seem to be relatively common at Ngogo and infanticide may be an important source of infant mortality in neighboring communities. Our observations cannot resolve questions about the sexual selection hypothesis. However, they are consistent with the range expansion hypothesis: the infanticides occurred during a period of frequent encounters between communities associated with a mast fruiting event, and Ngogo community members greatly increased their use of areas near the attack site during another mast fruiting event one year later. Our observations contribute to growing evidence that lethal intergroup aggression is a common characteristic of wild chimpanzee populations.     

Changes in female reproductive condition following male take-overs in a colony of hamadryas and hybrid baboons

This paper describes and discusses events observed in the Madrid colony of hamadryas and hybrid baboons, when a novel group of 3 adult males, 3 adult females and 1 unweaned infant was introduced to the resident colony comprising 12 adult females, 11 juveniles and 6 unweaned infants. Novel males took over resident adult females in any reproductive condition, and all acyclic females (i.e. lactating, pregnant and immature) exhibited a dramatic enhancement of sexual activity. Lactating females shortened their postpartum amenorrhoea periods and resumed oestrous cycles around day 14 following the introduction of the novel males, without infanticide occurring. Their return to breeding condition was not affected by the age of their current infant or the day they were taken over by the males. A female in an early stage of pregnancy aborted spontaneously and resumed oestrus on day 26. The other pregnant female significantly shortened her gestation time, delivered a viable infant on day 13, and resumed breeding activity 39 days post-partum (on day 52), while suckling her infant. A cycling female adopted and suckled a 74-day-old infant, continued showing oestrous cycles and conceived. Immature females reached menarche significantly earlier than expected and only then joined one of the newly established harem units. It is argued that the observed enhancement of sexual activity was not imposed by the males' aggressive behaviour but rather was a spontaneous female response to male novelty. This single causal factor was potent enough to override the role that nutrition and lactation normally play in the control of the females' reproductive activity. Differences in latency until the appearance of the response were probably due to the different constraints imposed by the female's current reproductive state. It was also hypothesized that when (a) sexual swellings are attractive to males, (b) novel males are especially active in the process of bonding with new females, and (c) males are important sources of coalitionary support, females might by developing sexual swellings compete more successfully against other females and attain a higher position in the female hierarchy of the newly established unit. This would have the ultimate effect of increasing their potential reproductive success. In several cases females did gain socially by coming into oestrus, but attained no immediate reproductive advantage.