Behavioral and Hormonal Analysis of Social Relationships Between Oldest Females in a Wild Monogamous Group of Common Marmosets (Callithrix jacchus)

Social organization in common marmosets (Callithrix jacchus) appears to be based on a hierarchy of dominance, in which dominant females limit the reproductive functioning of subordinates. Reduced fertility was documented for captive but not for wild females. We investigated social dynamics and hormonal profiles of females living in a wild group. We collected behavioral and hormonal data during 7 mo from the reproductive and two nonreproductive adult females (probably daughters), and their interactions with the reproductive male. The subjects lived in a monogamous group at Nísia Floresta field station in northeastern Brazil. We collected behavioral data as all day follows, once a week and fecal material twice a week. We analyzed fecal samples for cortisol and progesterone using enzyme immuno assay (EIA) techniques. During the first three months we monitored the reproductive female (GRE) and the oldest nonreproductive female, (GIO). After the disappearence of GIO, we monitored the next oldest subordinate adult female, (GRA). GRE had just given birth at the beginning of the study, and she gave birth 6 mo later. During the last 2 weeks of GRE's gestation, GRA showed elevated progesterone levels, indicating ovarian cycling. Cortisol levels from GRE and GRA reached very high levels then. During GRA's cycling period, her interactions with the reproductive male (GT) were lower than when she was not cycling. We saw sexual interactions only between GT and GRE. The results provide evidence that ovarian function in mature subordinate females might be affected by the reproductive condition of the dominant female.     

Reproductive skew in female common marmosets: what can proximate mechanisms tell us about ultimate causes?

Common marmosets are cooperatively breeding monkeys that exhibit high reproductive skew: most subordinate females fail to reproduce, while others attempt to breed but produce very few surviving infants. An extensive dataset on the mechanisms limiting reproduction in laboratory-housed and free living subordinate females provides unique insights into the causes of reproductive skew. Non-breeding adult females undergo suppression of ovulation and inhibition of sexual behaviour; however, they receive little or no aggression or mating interference by dominants and do not exhibit behavioural or physiological signs of stress. Breeding subordinate females receive comparable amounts of aggression to non-breeding females but are able to conceive, gestate and lactate normally. In groups containing two breeding females,however, both dominant and subordinate breeders kill one another's infants. These findings suggest that preconception reproductive suppression is not imposed on subordinate females by dominants, at a proximate level, but is instead self-imposed by most subordinates, consistent with restraint models of reproductive skew. In contrast to restraint models, however, this self-suppression probably evolved not in response to the threat of eviction by dominant females but in response to the threat of infanticide. Thus,reproductive skew in this species appears to be generated predominantly by subordinate self-restraint, in a proximate sense, but ultimately by dominant control over subordinates' reproductive attempts.     

High rates of pregnancy loss by subordinates leads to high reproductive skew in wild golden lion tamarins (Leontopithecus rosalia)

Across taxa, cooperative breeding has been associated with high reproductive skew. Cooperatively breeding golden lion tamarins (Leontopithecus rosalia) were long thought to have a monogynous mating system in which reproduction was limited to a single dominant female. Subordinates with few reproductive opportunities delayed dispersal and remained in the natal group to provide alloparental care to siblings, thus allowing dominant reproductive females to meet the energetic needs associated with high rates of reproduction and successful infant rearing. The goal of this study was to re-assess monogyny in wild golden lion tamarin groups based upon pregnancy diagnoses that used non-invasive enzyme immunoassay for progesterone and cortisol, combined with weekly data on individual weight gain, bi-annual physical examinations noting pregnancy and lactation status and daily behavioral observations. We established quantitative and qualitative criteria to detect and determine the timing of pregnancies that did not result in the birth of infants. Pregnancy polygyny occurred in 83% of golden lion tamarin groups studied. The loss of 64% of subordinate pregnancies compared to only 15% by dominant females limited reproductive success mainly to dominant females, thus maintaining high reproductive skew in female golden lion tamarins. Pregnancy loss by subordinate adults did not appear to result from dominant interference in subordinate hormonal mechanisms, but more likely resulted from subordinate abandonment of newborn infants to mitigate dominant aggression.     

Post-conception reproductive competition in cooperatively breeding common marmosets

Common marmosets are cooperatively breeding monkeys that exhibit high female reproductive skew. Subordinate females usually fail to breed as a consequence of ovulation suppression and inhibition of sexual behavior, and, even when they do breed, typically rear fewer infants than dominants. We evaluated possible mechanisms of post-conception reproductive competition by comparing hormonal profiles across pregnancy, pregnancy outcomes, infant survivorship, and behavior in laboratory-housed families containing one (N=9) or two (N=7) breeding females. Breeding females in plurally breeding groups did not exhibit well-defined dominance relationships and rarely engaged in escalated aggression with one another. No significant differences were found among singly breeding mothers, plurally breeding mothers, and plurally breeding daughters in urinary chorionic gonadotropin or estradiol sulfate concentrations during pregnancy, fetal biparietal diameter, frequency of spontaneous abortion, frequency of stillbirths, number of live-born infants per litter, or infant mortality rates. When females gave birth while another female in the family was pregnant, however, their infants were highly likely to be killed. The perpetrator was definitively identified in only one family, in which a pregnant female killed her daughter's infant. These results are consistent with observations of free-living common marmosets and suggest that breeding females do not regularly influence one another's pregnancy outcomes, but that they may commonly kill each other's infants, especially during their own pregnancy. Our findings further suggest that infanticide by breeding females may have selected for the evolution of reproductive restraint in subordinate female marmosets.     

非优势顺位雄性黄山短尾猴的交配策略

在多雄多雌、顺位决定交配机会、雄性偏斜繁殖的非人灵长类社会中,低顺位雄性为提高自己的繁殖成功率,通常采取多样的交配策略以获得较多的交配机会。对非优势顺位雄性交配策略的研究可以增加对灵长类社会性行为复杂性的理解,对于深入探讨动物的婚配制度及繁殖策略具有十分重要的科学意义。本研究采用目 标动物取样法和全事件记录法,在２０１２ 年９ －１２ 月（交配期）记录了安徽黄山短尾猴鱼鳞坑ＹＡ１ 群中４ 只成年雄性个体的交配及有关的行为。研究发现：（１）非优势顺位雄性个体在远离优势顺位雄性视野范围的交配频次和交配时间显著高于优势顺位视野范围内;（２）与优势顺位雄性个体相比,非优势顺位雄性的强行交配（forced copulation）和隐秘交配（clandestine copulation）比例较高;（３） 就交配对象而言,对成功生育的雌性个体,优势顺位雄性在选择交配对象时具有明显的倾向性,非优势顺位雄性在选择时倾向性不显著;对未生育的雌性,优势顺位雄性更倾向于选择没有生殖经历的亚成年雌性个体,非优势顺位雄性则倾向于选择处于哺乳后期的成年雌性个体;（４）在具体交配策略上,优势顺位雄性选择跟随（follow） 雌性,非优势顺位雄性则通过做鬼脸 （grimacing）和性追求（sexual chasing）直接获取交配机会。本研究结果表明黄山短尾猴中非优势雄性个体形成了多变的交配策略,更多采取强制性方式,以获得更多的交配机会,多数的交配都是机会性的。     

Diminished maternal responsiveness during pregnancy in multiparous female common marmosets

Common marmoset monkeys (Callithrix jacchus) live in small groups in which, usually, only a single female breeds and all group members provide infant care. When two females breed concurrently, however, they may commonly kill one another's infants, especially during the peripartum period. To investigate the mechanisms underlying infanticide by breeding females, we characterized responses of multiparous females to infants and determined circulating hormone levels in adult females during early pregnancy, late pregnancy, and the early postpartum period. Additionally, we compared the responses of postpartum females to their own infants and infants of other females (unfamiliar infants). Postpartum females were highly maternal toward both their own and unfamiliar infants, and showed no differences in their behavioral or hormonal responses to the two. During both early and late pregnancy, however, these females exhibited longer latencies to initially approach unfamiliar infants and spent less time carrying unfamiliar infants. Moreover, females spent less time carrying unfamiliar infants during late pregnancy than early pregnancy. Most late pregnant females never carried infants, and those that did rejected them quickly. Prolactin concentrations were higher and progesterone concentrations lower postpartum than in early or late pregnancy, while estradiol concentrations, the estradiol-to-progesterone ratio, and cortisol levels were higher during late pregnancy. Within reproductive conditions, however, maternal behaviors were not correlated with hormone levels. These results suggest that maternal responsiveness in marmosets may be attenuated during pregnancy, especially late pregnancy, and this may contribute to infanticide by breeding females.     

Different ovarian responses to potential mates underlie species-specific breeding strategies in common marmoset and Goeldi's monkey

Callitrichids are cooperative breeders, characterized by obligate twinning, extensive paternal care, and monopolization of reproduction by the dominant female. This is the case in the common marmoset, and in common marmoset groups of more than one adult female, subordinate females are typically acyclic consistent with infertility. However, one callitrichid, Goeldi's monkey, gives birth to singletons and exhibits low paternal care. Given these reproductive traits of Goeldi's monkey, we hypothesized that there would not be suppression of ovarian activity. To test this hypothesis, we applied non-invasive endocrine methods in a step-wise experiment with laboratory groups of both species. In each species, six pairs of sisters were studied alone, in visual contact with an unrelated male and in a polygynous trio with the male, and urine samples were collected for determination of oestrogen titres reflecting ovarian activity. Common marmoset sister pairs exhibited a marked difference in social status: during the study 5 of 6 dominant females conceived but only 1 of 6 subordinate females; the remaining 5 subordinates were acyclic at the end of the study, and instances of ovulation typically resulted in aggression. Goeldi's monkey sister pairs showed no status differences: in all pairs, however, both sisters exhibited a temporary cessation of ovarian cyclicity on trio formation, followed by ovulation and conception. We conclude that these marked differences in ovarian responses reflect the differences in inter-female competition for paternal caregiving resources. In common marmosets with high inter-female competition, suppression of ovulation functions to reduce aggression received by subordinate females; in Goeldi's monkey with low competition, temporary cessation of ovulation could facilitate female choice.     

Two breeding females within free-living groups may not always indicate polygyny: alternative subordinate female strategies in common marmosets (Callithrix jacchus)

The mating system of callitrichids has been reported to be monogamous, polygynous and polyandrous. In Callithrix jacchus, groups with 2 breeding females and groups with 1 breeding female have been reported. Our purpose was to evaluate the occurrence of occasional reproduction by subordinate females in free-ranging C. jacchus groups characterized as monogamous. Four groups were monitored at a field site of IBAMA-Brazil for between 20 and 72 months. We recorded the birth of 7 sets of twins to subordinate females that had never reproduced before. Sexual activities were recorded opportunistically: dominant females copulated with only the resident male, while subordinates copulated with extra-group males. We suggest these were essentially monogamous groups that occasionally had 2 reproductive females. Between-group copulations seem to be an alternative strategy used by the subordinates. Despite the costs, there would probably be benefits as a result of scanning for vacancies for reproductive positions in neighbouring groups and the establishment of ties with extra-group males that might become a reproductive partner in the future.     

Ovarian function of pygmy marmoset daughters (Cebuella pygmaea) in intact and motherless families

Reproductive inhibition of subordinate Callitrichid group members has been shown to vary with genus; whereas female Leontopithecus subordinates have normal ovarian cycles and occasionally breed within groups, subordinate Saguinus females almost never do so, with Callithrix species showing intermediate levels of reproductive inhibition. No information has been available on patterns of reproduction or inhibition in subordinate females in the genus Cebuella. We assessed fertility in Cebuella pygmaea daughters to allow comparison with the remaining Callitrichid genera. Specifically, the project had two goals: 1) to determine if there was evidence of reproductive inhibition of daughters living in family groups, and 2) to compare the ovarian function of daughters living in intact family groups with that of daughters residing in motherless families (i.e., without the breeding female). We collected daily urine samples for 6–8 weeks from eight pygmy marmoset daughters living in intact family groups or motherless families. Determination of ovulatory cycling or reproductive quiescence depended on the hormonal profiles generated from urinary luteinizing hormone and pregnanediol-3-glucuronide concentrations. All females in the motherless condition (aged 13–30 months) (n = 4) ovulated during the study. In contrast, only one of four daughters (aged 13–20 months) residing in intact families was found to be cycling. Data from motherless groups indicate ovarian cycling may begin between 15 and 17 months of age. Reproductive inhibition occurs in pygmy marmosets, although in a pattern more similar to Callithrix than to other Callitrichid genera. Am. J. Primatol. 43:347–355, 1997. © 1997 Wiley-Liss, Inc.     

Costly reproductive competition between females in a monogamous cooperatively breeding bird

In many cooperatively breeding societies, only a few socially dominant individuals in a group breed, reproductive skew is high, and reproductive conflict is common. Surprisingly, the effects of this conflict on dominant reproductive success in vertebrate societies have rarely been investigated, especially in high-skew societies. We examine how subordinate female competition for breeding opportunities affects the reproductive success of dominant females in a monogamous cooperatively breeding bird, the Southern pied babbler (Turdoides bicolor). In this species, successful subordinate reproduction is very rare, despite the fact that groups commonly contain sexually mature female subordinates that could mate with unrelated group males. However, we show that subordinate females compete with dominant females to breed, and do so far more often than expected, based on the infrequency of their success. Attempts by subordinates to obtain a share of breeding impose significant costs on dominant females: chicks fledge from fewer nests, more nests are abandoned before incubation begins, and more eggs are lost. Dominant females appear to attempt to reduce these costs by aggressively suppressing potentially competitive subordinate females. This empirical evidence provides rare insight into the nature of the conflicts between females and the resultant costs to reproductive success in cooperatively breeding societies.     

Social organization in a wild population ofCallithrix jacchus: II. Intragroup social behavior

The social behavior of the common marmoset has been well studied in captivity, but little is known about the social dynamics of this species in its natural habitat. Social relationships were studied in three polygynous groups of common marmosets,Callithrix jacchus, in northeastern Brazil. Breeding adults appeared to be the center of social life and were the most frequent grooming partners or nearest neighbors for most adult group members. The observations of unidirectional agonistic interactions suggest that breeding adults were also dominant over all other group members, but that neither sex was dominant over the other. The dynamics of within-group social relationships are likely to be important determinants in the reproductive strategies employed by marmoset females.     

Behavioral discrimination between circumgenital odor from peri-ovulatory dominant and anovulatory female common marmosets (Callithrix jacchus)

Social peer groups of callitrichid monkeys [marmosets and tamarins] exhibit intrasexual dominance hierarchies in captivity. This laboratory study employed two-choice behavioral discrimination bioassys to test the hypothesis that scent from female common marmosets contains chemical cues that permit discrimination between dominant females in the peri-ovulatory versus luteal phase of the ovarian cycle and females holding dominant versus subordinate status. When scent from only dominant females was presented, marmosets directed significantly greater amounts of investigatory behavior toward peri-ovulatory scent versus scent collected during the luteal phase of the ovarian cycle. Animals of both sexes demonstrated significant discriminatory behavior between scent deposited by dominant versus subordinate females, but only when the dominant female was in the peri-ovulatory phase of the ovarian cycle. Test animals directed equal amounts of investigative behavior toward scent from luteal-phase dominant females and subordinate females. Female test subjects deposited significantly more scent marks over presented scents than did male subjects, particularly when the scent had been donated by a peri-ovulatory female. Chemical odors specific to the peri-ovulatory and luteal phases of the ovarian cycle may play a role in mediating behavioral interactions among marmosets. Am. J. Primatol. 46:265–284, 1998. © 1998 Wiley-Liss, Inc.     

Behavioral and Endocrine Responses in Male Marmosets to the Establishment of Multimale Breeding Groups: Evidence for Non-monopolizing Facultative Polyandry

Studies of wild callitrichids provide conflicting evidence regarding polyandrous groups. One perspective supports a monopolizing breeding strategy on the part of one male, while the alternative perspective suggests that polyandry does not lead to a breeding monopoly. We tested the hypotheses in male marmosets (Callithrix kuhlii) with 5 polyandrous groups composed of related/familiar males as our attempts to establish polyandrous groups of unrelated/familiar males failed. We monitored male social and sexual behavior and urinary testosterone (T) and cortisol (CORT) across the first 80 days of group formation and contrasted them with similar measures in males housed in monogamous groups. We also examined the same measures across the females' ovulatory cycles for polyandrous males. We found little evidence that males in polyandrous groups exercised a mating monopoly over the female and no evidence for overt competition between polyandrous males. We found 2 behavioral differences: polyandrous males were less often in proximity and copulated more often with the female than monogamous males did. Our findings suggest that the males in newly-formed groups of marmosets do not monopolize breeding and social behavior with the female. This appears to be the case for 3 reasons. First, males may use sperm competition rather than overt competition. Secondly, it may take longer for relationships to develop between the female and the males in polyandrous groups versus in monogamous groups. Thirdly, the cost of infant care is sufficiently high to demand that group members get along when groups are small and reproductive benefits are shared.     

Group size,composition, and reproductive success in wild common marmosets (Callithrix jacchus)

Data from published sources about size and composition of wild common marmoset groups (Callithrix jacchus) were analyzed to see if the number of juveniles in a group is closely related to the number of other group members. Mean group size was 8.7 members including 4.4 adults (1.8 females, 2.5 males), 2.9 subadults, and 1.4 juveniles. The number of juveniles was significantly positively correlated to the number of adult males. Groups with one or two adult males had significantly fewer juveniles (mean: 1:1 juveniles) than groups containing more than two adult males (mean: 2.0 juveniles). Apart from a different number of subadults, results showed obvious similarities between common marmosets and tamarins of the genus Saguinus in size and composition of subgroups of adults as well as the key role of adult males in mediating the reproductive success of a breeding female. Common marmoset females seem to gain direct fitness benefits in increased reproductive success from the presence of a larger number of adult males. Whether or not other group members get fitness benefits depends on the reproductive strategy of adult males (monogamy vs. polyandry), their kinship, and on the genetic relationship of nonbreeders to the offspring of the breeding female. © 1995 Wiley-Liss, Inc.     

Sociality, mating system and reproductive skew in marmots: evidence and hypotheses

Marmot species exhibit a great diversity of social structure, mating systems and reproductive skew. In particular, among the social species (i.e. all except Marmota monax), the yellow-bellied marmot appears quite different from the others. The yellow-bellied marmot is primarily polygynous with an intermediate level of sociality and low reproductive skew among females. In contrast, all other social marmot species are mainly monogamous, highly social and with marked reproductive skew among females. To understand the evolution of this difference in reproductive skew, I examined four possible explanations identified from reproductive skew theory. From the literature, I then reviewed evidence to investigate if marmot species differ in: (1) the ability of dominants to control the reproduction of subordinates; (2) the degree of relatedness between group members; (3) the benefit for subordinates of remaining in the social group; and (4) the benefit for dominants of retaining subordinates. I found that the optimal skew hypothesis may apply for both sets of species. I suggest that yellow-bellied marmot females may benefit from retaining subordinate females and in return have to concede them reproduction. On the contrary, monogamous marmot species may gain by suppressing the reproduction of subordinate females to maximise the efficiency of social thermoregulation, even at the risk of departure of subordinate females from the family group. Finally, I discuss scenarios for the simultaneous evolution of sociality, monogamy and reproductive skew in marmots.     

Sexual behavior and extragroup copulations in a wild population of common marmosets (Callithrix jacchus).

Sexual behavior and mating patterns are described for 3 free-ranging groups of common marmosets living in a coastal forest in northeastern Brazil. Each group contained 2 breeding females. Within groups, sexual behavior was generally restricted to breeding females and a single behaviorally dominant male. Of 101 mounts and copulations, 24 involved pairings of individuals from 2 different groups. Extragroup sexual behavior was performed by both breeding and nonbreeding group members, and 65% of all adults mounted or copulated with an extragroup individual at least once. Sexual behavior occurred throughout the female reproductive cycle but was significantly more frequent during an 11-day 'conception period'. Thus, while female marmosets show no physical signs of estrus, both males and females likely do have some information about the timing of ovulation. Mating patterns in this population included both polygyny and monogamy and varied between groups and over time.     

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.     

Hormonal correlates of development and natal dispersal in wild female owl monkeys (Aotus azarae) of Argentina

Pair-living and socially monogamous primates typically do not reproduce before dispersing. It is currently unclear whether this reproductive suppression is due to endocrine or behavioral mechanisms. Cooperatively breeding taxa, like callitrichids, may forego reproduction in natal groups because they reap inclusive fitness benefits and/or they are avoiding inbreeding. However, neither of these benefits of delayed reproduction appear to adequately explain the lack of reproduction prior to leaving the natal group in pair-living monogamous species. In this study, we determined whether wild Azara's owl monkeys (Aotus azarae) in the Argentinean Chaco establish reproductive maturity prior to dispersing. We utilized 635 fecal extracts to characterize reproductive hormone profiles of 11 wild juvenile and subadult females using enzyme immunoassays. Subadult females showed hormone profiles indicative of ovulatory cycling and had mean PdG and E1G concentrations approximately five times higher than juveniles. Contrary to expectations from the inbreeding avoidance hypothesis, female owl monkeys do not delay puberty, but rather commence ovarian cycling while residing in their natal group. Still, subadults appear to have a period during which they experience irregular, non-conceptive cycles prior to reproducing. Commencing these irregular cycles in the natal group may allow them to develop a state of suspended readiness, which could be essential to securing a mate, while avoiding costs of ranging solitarily. Our results indicate that reproductive suppression in female owl monkeys is not due to endocrine suppression. We suggest that adults likely use behavioral mechanisms to prevent subadults from reproducing with unrelated adult males in their natal group.     

Polygynandry in a red fox population: implications for the evolution of group living in canids?

Canid social groups are typically thought to consist of extendedfamilies, that is, a dominant breeding pair and related nonbreedingsubordinates, that principally obtain indirect fitness benefitsfrom helping to raise the offspring of the dominant pair. Consequently,the monogamous pair has been viewed as the basic fundamentalunit of canid social organization. However, there have beenfew genetic studies that have tested this assumption. We analyzedthe parentage of red foxes (Vulpes vulpes) in a high-density(19.6–27.7 adult foxes/km²) population in Bristol, UK,to determine (1) whether groups typically produced a singlelitter of cubs annually and (2) whether male and female foxesexhibited monogamous mating strategies. Social monogamy (theproduction of one litter in a social group) was observed orassumed in 54% of breeding attempts (N = 13 group-years). However,polyandrous and polygynous patterns of mating were common. Multiplepaternity was confirmed in 38% of litters (N = 16) containingoffspring with resolved maternity and paternity (N = 30 cubs);when including cubs with unresolved paternity (N = 20), multiple-paternitymay have occurred in 69% of litters. Litters were sired by anaverage of 1.6 identified males (range = 1–4); when includingcubs with unresolved paternity, litters may have been siredby up to seven males. Only 20% (6/30) of cubs with resolvedmaternity and paternity were sired by males within the socialgroup. Within groups, dominant females did not breed with subordinatemales; dominant males did breed with subordinate females. Dominantand subordinate females both produced cubs with dominant andsubordinate males from other social groups. Mean adult relatednessin groups typically ranged from 0.15–0.35, indicativeof second-order rather than first-order relatives.