“Following,” an Alternative Mating Strategy Used by Male Olive Baboons (Papio hamadryas anubis): Quantitative Behavioral and Functional Description

Recent data reveal that high-ranking males are unable to monopolize sexual access to fertile females, suggesting the potential evolutionary significance of alternative strategies across many taxa. We examined a well known behavior, “following” of a consortship by adult male olive baboons (Papio hamadryas anubis), that has received little empirical attention. Four consort takeover tactics have been suggested, for both follower and nonfollower males: takeover of an abandoned consort female, individual aggressive challenge to oust the consort male, coalitionary challenge to oust the consort male, or an opportunistic consort takeover relying on the consort male being distracted. We addressed the following questions: 1) How does the behavior of followers differ from nonfollowers? 2) Is following an effective alternative mating strategy? 3) What tactics do followers use to obtain access to fertile females? 4) Do dominance rank and female cycle day influence tactic expression? We studied two habituated groups of olive baboons from September 2009 to July 2010 in Kenya. Followers had a higher rate of agonistic interactions with the consort male and affiliative interactions with other followers. Overall, 74% of consort takeovers were executed by follower males of the targeted consortships. Each of the four consort takeover tactics were used by both follower and nonfollower males, although followers used the individual aggressive challenge and coalitionary challenge tactics more often than nonfollowers. Dominance rank, but not female cycle day, influenced the expression of consort takeover tactics. Our findings indicate that following provides males with sexual access to females.     

Mating Tactics in Male Grey-Cheeked Mangabeys (Lophocebus albigena)

Reproductive tactics of males can change with individual quality, relatedness and social structure. Here we describe the behaviours of male grey-cheeked mangabeys towards other males, and females and their offspring ( Lophocebus albigena ) in relation to male status (high-ranking/low-ranking/transient) and group composition in Kibale National Park, Uganda. High-ranking males had the highest mating success, frequency of loud calls, mate guarding and aggression towards females and males. Only transient males were often observed to be aggressive towards juveniles, while some high-ranking males provided infant care. Mating tactics of high-ranking males varied greatly among the five studied groups, probably as a function of the intensity of male–male competition. These results are discussed with regard to the role of male–male competition and behaviours that could affect female mate choice as tactics to obtain reproductive success.     

Mate Choice in Non-Human Primates

Mate choice has been observed in many species of non-human primates.There are few definitive studies, however, due to the long lifespans, complex social behavior, and cognitive abilities of theseanimals. Here I review the current literature on mate choicein primates. Females typically prefer complex behavioral traitssuch as social status, familiarity, personality, and parentalcare abilities. This tendency to prefer behavioral traits isconsistent with the non-primate mammalian data. A female's abilityto express preferences, however, is often constrained by hersocial environment—in particular male mating tactics andfemalefemale competition. Males exhibit preferences for high-ranking females. In severalspecies, high-ranking females produce more offspring than low-rankingfemales. In addition, females may also influence male dominancerank and in doing so reduce male-male competition and increasemale mating success.     

Relatedness in wild chimpanzees: influence of paternity, male philopatry, and demographic factors

In chimpanzees (Pan troglodytes), high-ranking males are expected to have high reproductive success and females typically emigrate upon reaching maturity. Although high average relatedness among males in the same social groups has been assumed, previous reports have indicated that relatedness among males is not necessarily significantly higher than that among females. The paternity of 11 offspring and the relatedness of 50 individuals in the M group of chimpanzees at Mahale Mountains National Park, Tanzania, were investigated using DNA analyses. We determined the fathers of 10 offspring. Two different alpha males sired a total of five offspring, whereas the other males had low reproductive success. The proportion of paternal half-sibling pairs among the 10 offspring was 15.6%. The average relatedness among mature males was significantly higher than that among mature females. The existence of an old male and the long tenure of one alpha male may have contributed to this significant difference. The average dyadic relatedness among mature natal individuals was significantly higher than that in natal-immigrant pairs in which the individuals came from different groups. The average relatedness among immigrant females was similar to that in pairs of natal and immigrant females, suggesting that the immigrants came from various groups. Thus, female transfer acts to maintain low average relatedness within the group. A comparison of our results to those from other study sites suggests that although the average relatedness among adult males does not reach the level of half-siblings, under some circumstances it can exceed the relatedness of females.     

Changes in the dominance rank and reproductive behaviour of male bonnet macaques (Macaca radiata)

The dominance rank of male bonnet macaques influenced their associations and sexual interactions with cycling and conceiving females. Only high-ranking males formed exclusive associations with high-ranking females, and high-ranking males copulated with these females more often than did other males. Changes in male dominance rank were directly related to changes in male mating behaviour, as males who rose in rank spent increasing amounts of time in exclusive proximity to conceiving high-ranking females, and males whose ranks declined spent decreasing amounts of time in proximity to such females. The year of the study in which dominance relationships were most stable was also the year in which the top-ranking male most successfully monopolized access to conceiving high-ranking females.     

Male takeover in Colobus vellerosus at Boabeng-Fiema Monkey Sanctuary, central Ghana

We describe a case of male takeover in the ursine black-and-white colobus (Colobus vellerosus). In April 2001, an all-male group attacked and eventually invaded our uni-male study group. Aggression increased following the takeover and the former resident male, severely wounded, became peripheral. The youngest immature received severe aggression from the new males but survived. The immatures mother intervened in most instances of this aggression. Eventually, the former resident male re-established relationships with some of the females and concurrently intervened to protect the immature. Defeated males that stay in their group can contribute to the protection of infants born during their tenure from infanticidal males. The females mated with the new males. Takeovers may be a means by which males acquire groups of females in C. vellerosus.     

Distribution of affiliative behaviors among adult females within a group of wild patas monkeys in a nonmating,nonbirth season

The distribution of four affiliative behaviors (proximity within 3 m, allogrooming, contact calling, and co-night-resting) were examined in a group of wild patas monkeys (Erythrocebus patas) during a nonmating, nonbirth season. To a greater or lesser extent, dominance rank and kinship influenced these behaviors of the adult females. Since high-ranking females tended to exhibit some of these behaviors with high frequency, they were considered to be acting as the focus of affiliative behaviors and as the center for group cohesion. Furthermore, related adult females also tended to exhibit some of these behaviors with a high frequency toward one another, so that matrilineal kinship was also seen to be an important factor for group cohesion. In contrast, the harem male tended to exhibit these behaviors at a low frequency and/or had no affiliative partner for any of them. Thus, it appears that the social organization of the patas group is concentric, being composed of high-ranking females in the center, low-ranking females at the periphery, and the harem male at the distant periphery.     

Mother — Offspring Conflict in the Saharan Arrui,Ammotragus lervia sahariensis: Relation to Weaning and Mother's Sexual Activity

Behavioural conflict between mother and offspring was investigated in a captive population of the Saharan arrui (Ammotragus lervia sahariensis, Artiodactyla: Bovidae). The frequency of agonistic behaviours (mother's aggressiveness and calf's retreats) and unsuccessful suckling attempts, Hinde's proximity index and the distances between mother and calf have been analysed in relation to weaning and sexual activity of the mother. Mothers that conceive in the following mating season accelerate the weaning process of their current offspring; furthermore, high-ranking females wean their male calves earlier. Behavioural conflict occurs during the resumption of the mother's sexual activity; however, no conflict appears to happen during weaning.     

Female choice impacts resident male takeover in golden snub-nosed monkeys(Rhinopithecus roxellana)

In primate species with social systems consisting of one-male breeding units(OMUs), resident male takeover represents a major challenge to individual reproductive success and mating strategies. The golden snub-nosed monkey(Rhinopithecus roxellana)is characterized by large multilevel societies(MLS)comprised of several OMUs and all-male units(AMUs);however, the factors and mechanisms associated with resident male takeover, which offer important insight into primate reproduction and social strategies, are still poorly understood. Based on 5-year monitoring data from a free-ranging herd of golden monkeys from the Qinling Mountains in China, we categorized three phases of an OMU, that is, a rising phase,developing phase, and declining phase. The rising and declining phases were unstable periods in which male takeover in an OMU might occur. Factors causing takeover, such as leader male rank, fighting ability, reproduction rate, and affiliation(proximity,allogrooming), were analyzed for males and females and for different OMUs. Results indicated that the new resident male's fighting ability was lower than that of the former resident male in 23 cases. After replacement, the rank order of the new resident male significantly declined. Females involved in a takeover increased their distance from the resident male and decreased mating frequency during the three months prior to takeover. Females with infants under one-year-old had a marked effect on the specific time of takeover occurrence. These results suggested that female choice was the main factor deciding whether a takeover attempt was successful. Furthermore, rather than male conflict, females more often initiated and affected takeover and outcome, implying that the social status and competitive ability of the males played lesser roles during takeover.     

Abortion following the immigration of an adult male baboon (Papio cynocephalus)

Three abortions and the death of a vigorous infant occurred in a baboon (Papio cynocephalus) group in Amboseli National Park, Kenya, within the two weeks following the immigration of an aggressive adult male. The immigrant male attained top-ranking dominance status in the group prior to these events. Circumstantial observations suggest that the reproductive losses were related to persistent intense aggression from the immigrant adult male. In the past ten years, only three other miscarriages have occurred in Amboseli. Inducement of abortion is discussed as a reproductive tactic that may be available to males of mammalian species whose life histories favor the evolution of infant-killing by males.     

Male dominance rank and reproductive success in an enclosed group of Japanese macaques: with special reference to post-conception mating

The mating behaviour and reproductive success of male Japanese macaques (Macaca fuscata) were studied in relation to the female sexual cycles, which were monitored from the plasma profiles of gonadotropins and ovarian hormones. Based on observations of the mating behaviour during four successive mating seasons and paternity identification by DNA fingerprinting in 35 out of 37 offspring born in the subsequent birth seasons, the correlations between (1) male dominance rank and timing of mating, and (2) male dominance rank and reproductive success were examined. The results may be summarized as follows. (1) The number of copulations with ejaculation by any male was positively correlated with the male dominance rank, but not with the identified numbers of offspring fathered by each male. (2) Males could not choose ovulatory females as mating partners: the number of copulations with ejaculation with females during ovulatory weeks was not related to the male's rank. Monopolized copulations in consortship were mostly observed between high-ranking males and non-lactating parous females after conception. (3) Paternity testing showed that the male copulating most frequently with a female was not the identified father in 11 out of 15 cases. Prediction of the fathers of offspring was difficult even from the number of copulations occurring at around the estimated time of ovulation. An adaptive explanation of these correlations is discussed.     

Dominance Rank and Parental Investment in Swine (Sus scrofa domesticus)

Using domestic swine, we tested the general prediction from life history theory that females increase their investment in offspring with increasing age and parity. Because increased investment may have a greater beneficial impact on the lifetime reproduction of sons than daughters, we also tested the prediction that older females would invest more in sons than in daughters compared to younger females. Finally, we examined whether age- or parity-related patterns of change in reproductive effort were associated with differences in the social dominance ranks of females. Female swine from a large number of domestic breeds were assigned to social groups, and their dominance ranks were determined based on the outcome of agonistic encounters. The prediction that older females produce larger litters was supported, but the increase was related only to age, not to parity. Across all ages, high-ranking females produced a greater proportion of sons than low-ranking females. Contrary to our prediction, there was no rank-related change in the proportion of sons born with increasing age or parity. However, the mean body masses offspring born to high-ranking females increased with increasing maternal age and parity, but this was not the case for offspring of low-ranking females. Studies of free-ranging groups of swine are needed to determine whether an increase in body mass at birth would have different effects on the reproduction of sons or daughters.     

Origin and fate of a one-male savanna babbon group formed by fissioning

An adult male chacma baboon,Papio hamadryas ursinus, emigrated from his habituated natal group at age 100 months and joined a neighboring multimale-multifemale group. Subsequently this male, together with eight adult females, all with infants <1 year old, formed a one-male group (OMU). The male was the only adult male in this group for over 200 days. Circumstantial evidence shows that shared parentage of the infants with this male determined which females joined the new group. In addition, 10 juveniles younger than 4.5 years joined the new group. Based upon persistent close physical association, especially at sleeping sites, these juveniles were presumed to be the older independent progeny of the eight adult females. Thus, the founding elements of the new group were the adult male and partial matrilines—mothers, their infants, and their independent juvenile offspring. The OMU status of the group ended with the sequential intrusion of three males known to be low ranking in other groups. The first of these intruders was successful in joining the OMU in spite of the OMU male's earlier successes in rebuffing this and other potentially high-ranking males. Six additional males later entered the fission group during a 6-month interval. Two of them outranked the original male. All additional males present in the last 100 days of observations came from the same group, which was not the group of origin of the females.     

Impact of male takeover on intra-unit sexual interactions and subsequent interbirth interval in wild Rhinopithecus roxellana

Data were collected on sexual interactions before and after a male takeover of a one-male unit (OMU) of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, China. The original unit consisted of an adult male, 2 adult and 2 subadult females, 2 female juveniles and a single infant. Following the takeover, the new resident male copulated with 1 adult female, which was not lactating. Subsequent to the disappearance of her infant, the second (lactating female) entered breeding condition and began to solicit copulation with the new resident male. The subadult females also engaged in matings with the new male. The new resident male was observed mating, on 3 occasions, with females in 2 other OMUs. These are the first observations of sexual behaviour in free-ranging Sichuan snub-nosed monkeys after an OMU takeover. Sexual interactions play an important role in establishing relationships between the new male and resident females in the OMU.     

Male Dominance Rank,Female Mate Choice and Male Mating and Reproductive Success in Captive Chimpanzees

Mating and consequently reproductive success in male vertebrates are predominantly determined by intermale competition and female mate choice. Their relative importance however, is still poorly understood. We investigated the interrelationship between male dominance rank — a formal indicator of male competitive ability — female mate choice, and male mating success in a multimale-multifemale group of captive chimpanzees. In addition, we examined the relationship between male dominance rank and reproductive success determined by genetic paternity analysis over a 13-yr period in the same captive population. We related the frequencies of sociosexual behaviors to the female anogenital swelling stage and female fertile phase as determined by urinary and fecal progestogen analysis. Rates of behaviors in both sexes increased with increasing intensity of female swelling, but they were not influenced by the timing of the fertile phase. Male mating success was clearly related to male dominance rank, with high-ranking males performing the overwhelming majority of copulations. This was mainly due to both rank-related rates of male soliciting behavior and intermale aggressiveness during the period of well-developed female anogenital swelling. Although females solicited copulations mainly from the high-ranking males and thus expressed a mate choice based on rank, their overall contribution in initiating copulations and thus influencing male mating success was low. The data on paternity from the population, which always contained 4 adult males, revealed that -males sired the majority (65%) of offspring. We conclude, that male dominance rank is an important determinant of male mating and reproductive success in captive (and presumably wild) chimpanzees and that female mate choice is of minor importance in modulating male reproductive outcome.     

Trans‐generational effects of maternal rearing density on offspring development time in a parasitoid wasp

Maternal pre‐reproductive experience can impose phenotypic changes on offspring traits. These modifications may result from physiological constraints, although they can also increase the adaptation of offspring to their anticipated environment. Distinguishing between the two interpretations is often difficult. The effects of virgin female rearing density on their longevity and the characteristics of their male offspring are explored in the polyembryonic parasitoid wasp Copidosoma koehleri (Blanchard) (Encyrtidae: Hymenoptera). High rearing density may adversely affect maternal physiology or, alternatively, act as a cue for anticipated competition during the lives of the mothers and their offspring. Male offspring of group‐reared females reach pupation significantly sooner than male offspring of females reared alone. This accelerated development may provide an advantage when competition from superparasitising individuals is expected. The lifespan of high‐density females is longer than that of singly‐reared females, and their male offspring survive longer, suggesting that crowded rearing does not reduce the fitness of females or offspring. The shortened development time of male offspring may reflect an adaptive epigenetic response to predicted competitive conditions.     

Influences of female partner preference on potential reproductive outcome in Japanese macaques.

The immediate effects of female partner preference on male mating behaviors and its potential influence on male reproductive success and conception in the Japanese macaque (Macaca fuscata) were analyzed. Although male dominance interactions probably led to low-ranking males having more single-day consortships and high-ranking males more multi-day consortships, dominant males were unable to prevent females from mating with preferred subordinate males. Ultimately, there was no marked difference in the number of estimated offspring sired. Females chose not to mate with certain males and actively mated with others, suggesting that female partner preferences do affect conception. Evidence for this was found in paternity estimates, which reflected observed preferences for particular middle-ranking young adult males.     

Female rank and reproductive success among arashiyama B Japanese macaques (Macaca fuscata)

Five hypotheses that related female rank and reproductive success were tested in an intact troop of free-ranging, provisioned, Japanese macaques. The hypotheses stated that high-ranking females (1) begin parturition earlier in life than low-ranking females; (2) produce more offspring than low-ranking females; (3) give birth during some optimal time during the birth season to a greater extent than low-ranking females; (4) experience less infant mortality than low-ranking females;and (5) more frequently produce male offspring, while low-ranking females more frequently produce female offspring. A statistical analysis of the data which included three birth seasons and 55 adult females and 34 pubescent females, all of known age, rank, and matrifocal membership in the Arashiyama B troop, revealed few significant results. An association was found between the rank of the matrifocal unit and the age of first birth. However, the relationship was the reverse of hypothesis 1, i.e., females of the lower-ranking matrifocal units began parturition earlier than females of higher-ranking matrifocal units. Therefore, in this troop of Japanese monkeys— where alternative feeding strategies existed— there was little association between female rank and reproductive success.     

Determinants of Paternity Success in a Group of Captive Vervet Monkeys (<Emphasis Type="BoldItalic">Chlorocebus aethiops sabaeus</Emphasis>)

Paternity success of high-ranking primate males is affected by the number of males and the number of fertile females and their cycle synchrony. Female vervets in the wild show strong reproductive seasonality and do not advertise the ovulatory period with conspicuous signals or behavior. Because this makes it difficult for males to monopolize fertile females, it can be expected that male reproductive skew in this species is lower than in other cercopithecines living in multimale groups that advertise the ovulatory period. We assessed male reproductive success in a captive vervet group, initially consisting of 4 males and 12 unrelated females. Besides a general low reproductive skew, we predicted paternity success of the alpha males to be dependent on the overlap of synchronously fertile females, month into alpha male tenure, and housing conditions (the subjects were kept in a large park but had to be locked in a small indoor compartment during the winter months). Further, because the number of males reaching their prime increased over time, we predicted a decrease in reproductive success of the alpha male with increasing tenure length of the alpha male. To assess this we collected genetic samples from 27 of 32 offspring born into the group during 3 yr, using 7 polymorphic human microsatellite markers. Contrary to our predictions, reproductive success of the males occupying the alpha position during the study was among the highest found in cercopithecines, with the alpha males siring 78% of all offspring. The degree of overlapping fertile periods did not affect paternity success, nor did paternity success of the alpha male differ between the 2 housing conditions. Only the alpha male’s tenure length had an effect. Alpha male reproductive success decreased over time, which we attribute to either a shift in female mate choice toward younger males or to increased competition among the males in the later stage of the alpha male’s tenure. This study demonstrates the importance of assessing reproductive success of males throughout >1 season and should spawn more research into the role of female choice and postcopulatory mechanisms in this species.     

Costs of and Investment in Mate-Guarding in Wild Long-Tailed Macaques (Macaca fascicularis): Influences of Female Characteristics and Male–Female Social Bonds

Male primates living in multimale groups tend to direct mate and mate-guarding choices toward females of high reproductive value, i.e., high-ranking, parous females, or females with which they share strong bonds. Little is known, however, about the constraints that may limit male mate-guarding choices (the costs of this behavior) and the influence of the females’ quality on male investment in mate-guarding. We aimed to study the effects of female rank, parity status, and male–female social bond strength on the costs of and investment in mate-guarding by males. We carried out our study during two reproductive seasons on three groups of wild long-tailed macaques in Indonesia. We combined behavioral observations on male locomotion and activity with noninvasive measurements of fecal glucocorticoids (fGC). Males spent less time feeding when mate-guarding nulliparous females than when mate-guarding parous females and tended to have higher fGC levels when mate-guarding low-ranking nulliparous females than when mate-guarding high-ranking nulliparous ones. Evolution should thus favor male choice for high-ranking parous females because such a decision brings benefits at proximate (reduced costs of mate-guarding) and ultimate (higher reproductive value) levels. Further, male investment in mate-guarding was flexible and contingent on female reproductive and social value. Males were more vigilant and more aggressive toward other males when mate-guarding females to which they were strongly bonded and/or high-ranking ones than when mate-guarding other females. Our findings bring a new dimension to the study of mate choice by showing that males not only mate preferentially with high-quality females but may also aim to secure paternity with these females through optimized monopolization.