Why dominants do not consistently attain high mating and reproductive success: A review of longitudinal Japanese macaque studies

There is wide interest in the effects of reproductive biology, mating partner preference, and rank on mating success (MS) and reproductive success (RS) in primates. In particular, theory stresses importance on the mechanisms for attaining RS. Most theory hedges on competitive ability and priority of access to resources, whether they be food or estrous females. However, the majority of data used in favor of such hypotheses come from relatively short-term studies. We review these hypotheses based on long-term data from provisioned and unprovisioned populations of Japanese macaques. Neither MS nor RS were consistently attained by high-ranking males and females. For males, female choice and mating partner preference is seen to over-ride most male-male competitive behaviors likely to affect MS and RS through priority of access to estrous females. Long-term mating patterns driven largely by female partner preferences, results in decreasing MS and RS for older higher-ranking males. The long-term trend for females to prefer less familiar or novel partners results in higher MS and RS for younger, middle-ranking males. The effects of this vary according to troop size and the duration of male tenure. For females, no consistent trend was recognized for rank related RS in either provisioned or unprovisioned troops. Non-reproductive mating may provide differential benefit to high-ranking females for access to limited food resources in some habitats but overall the relationship was inconclusive. Distribution and defendability of food resource, rather than provisioning per se may be more important.     

Caring claims and the relational self across time: grandmothers overcoming reproductive crises in rural China

Revisiting the notion of relational personhood from a Chinese perspective, this article explores the premises of exchange underlying discourses of care, reproduction, and kinship in anthropology. Grandmothers contribute much of the care needed for reproduction of the next generation of children in the Chinese countryside. Their motivation to contribute care to secure offspring stems from the frustration of their past familial desires, and their hopes for transcendence through reproduction in the future. Grandmothers secure claims to offspring through their care between the interstices of the state bureaucracy and patrilineal norms. This care is not simply nurturing but can also become coercive and competitive. As Chinese grandmothers overcome past reproductive hardships by claiming future offspring through care, their selfhood not only becomes distributed through exchange with others, but also is dispersed across time in relation to past experiences and future aspirations of the self.     

Effectiveness of experiential learning with empowerment strategies and social support from grandmothers on breastfeeding among Thai adolescent mothers

Background

Grandmothers are important to successful breastfeeding because their knowledge, attitudes and experiences influence adolescent mothers’ decision to initiate and to continue breastfeeding. The purpose of this study was to assess the effectiveness of an experiential learning with empowerment strategies and social support (ELESSS) programme for grandmothers according to improvements in the rate and duration of exclusive breastfeeding (EBF); knowledge and attitude (KA) regarding breastfeeding; and perceived social support among adolescent mothers.

Methods

A quasi-experimental study was conducted in two hospitals, Banmi as an intervention hospital and Inburi as a control hospital, between May 2015 and March 2016. Forty-two pairs of adolescent mothers and grandmothers were recruited from each hospital. At the baseline, grandmothers in the intervention group attended 2 days of an ELESSS programme, and they attended a refresher course 2 and 4 months after delivery. The grandmothers in the control group and adolescent mothers in both groups received the routine programme. Participants were assessed at the baseline and at two and 6 months after delivery to determine the rate and duration of EBF, KA regarding breastfeeding and perceived social support.

Results

Adolescent mothers in the intervention group had the EBF rate at 6 months of around 29%, whereas the control group had the EBF rate at 6 months of about 5%, and the proportion of EBF in the intervention group was six times that of the control group. The median EBF duration in the intervention group was 90 days, while the control group was 0 day. A repeated measure ANOVA analysis showed that the intervention group’s participants had significantly better knowledge and attitudes towards breastfeeding, while the adolescent mothers in the intervention group had a significantly higher perceived level of social support.

Conclusion

The ELESSS programme proved to be effective in increasing the rate and duration of EBF in adolescent mothers. Grandmothers are key to promoting, protecting and supporting breastfeeding.

Trial registration

ClinicalTrials.in.th: TCTR20161001002

     

The development of peer-mate relationships in Japanese macaque infants

The play behavior of Japanese macaque infants was studied for 6 months at Arashiyama, Japan. Three types of play were identified. The first (solitary play) was observed in five to 12-week old infants. The second type of play (parallel play) was observed in infants from 12 to 21 weeks old. After the 12th week, the third type of play (associate play) was seen. At this point the infants seldom played without partners. It is in associate play that dominant and submissive behavior may be seen, and from which dominance relations may be assumed. It is said that the rank of a 12 week-old infant parallels that of its mother.     

Radiation and phylogeography in the Japanese macaque, Macaca fuscata

The Japanese macaque (Macaca fuscata) presumably differentiated from eastern rhesus macaque (Macaca mulatta) populations during the Pleistocene and the two species are closely related. In order to analyse speciation and subspeciation events in the Japanese macaque and to describe historical and current relationships among their populations, we sequenced and analysed a fragment of 392bp of mitochondrial DNA (mtDNA) control region in 50 individuals belonging to six populations of Japanese macaque and compared these sequences with 89 eastern rhesus macaque control region sequences from GenBank/EMBL database. There were high genetic similarities between both species and only two positions were fixed within each species, which supports the inclusion of the Japanese macaque in a single species with eastern populations of rhesus macaques. Japanese macaque ancestors colonised Japan after the separation of the two species, estimated at between 0.31 and 0.88 million years ago (Mya). The star-like phylogeny, multimodal mismatch distribution, and lack of correlation between geographic and genetic distances are in accordance with a rapid dispersion of macaques throughout the archipelago after the arrival into Japan. The species shows low genetic variation within populations and high levels of genetic differentiation among populations with no mtDNA haplotype shared across populations. Genetic distances between Yakushima macaques (Macaca fuscata yakui) and any other population of Macaca fuscata fuscata subspecies are comparable to the distances between populations of Honshu, Awajishima, and Kyushu, not supporting the classification of Yakushima macaques as a different subspecies.     

Sex differences in body fat parameters from the early reproductive to the postreproductive period of life: a multivariate analysis

Sex diversity has been observed for many body parameters, and special attention has been paid to changes during puberty and menopause. In the present study we performed a multivariate analysis on several body fat parameters to obtain a synthetic overview of sex differences from the early reproductive period to the postreproductive period. The sample study is composed of 373 healthy Italian adults (294 females and 79 males). We have examined the amount of fat (in kilograms, as measured by dual-energy x-ray absorptiometry) in the left arm, left leg, left trunk hemisphere, right arm, right leg, and right trunk hemisphere, waist to hip ratio, and BMI. The sex differentiation from the early reproductive to the postreproductive period of life has been based on differences between the position of male and female centroids on the discriminant functions obtained for various periods of life. The difference between males and females increases suddenly after 20 years, reaching a maximum at 30 years. In the period between 30 and 40 years the difference decreases quickly, and after 40 years the difference is relatively small and remains practically constant. The fact that maximum sex differentiation coincides with age of best reproductive efficiency points to a relationship between the body parameters investigated and hormone production related to human reproduction.     

The reproductive cycle of the crab-eating macaque (Macaca fascicularis)

Characteristic changes in the menstrual cycle of the crab-eating macaque were evaluated. Cyclical changes in type and abundance of exfoliated cells in vaginal smears as well as the ferning pattern of cervical mucus were observed. These indices were useful in predicting approximate ovulation time. The cyclical changes in sexual skin swelling and/or coloration were detected only in adolescent females. Micro-sections from ovaries of autopsied animals revealed large Graafian follicle formations often rupturing by day fourteen of the cycle. Length of the menstrual cycle ranged from 26–38 days with a modal value of 28 days.This research has been supported by Ford Foundation Grant No. 710-0287.     

Evolution of the ABO blood group gene in Japanese macaque

We determined 5 sequences of Japanese macaque ABO blood group gene exon 7 (ca. 0.5 kb) and 2 sequences for exon 5 and intron 6 (ca. 1.7 kb). We compared those data with published sequences of other Old World monkey species, and the results suggest that alleles A and B were polymorphic in the ancestral species of macaques, and that B type allele evolved independently in macaque and baboon lineages.     

Ovarian cycle phase and same-sex mating behavior in Japanese macaque females

The relationship of the ovarian cycle phase to same-sex mounting activity in adult female Japanese macaques (Macaca fuscata) was studied during the 1997/1998 mating season. Fecal samples were collected from eight female subjects two to three times per week and analyzed by enzyme immunoassay for fecal hormone levels. Hormone profiles of estrone (E1) and pregnanediol (PdG) were used to separate ovarian cycles into three phases: follicular, periovulatory, and luteal. Patterns of same-sex and heterosexual mounting behavior in the females were analyzed for phase variation during conceptive cycles. Same-sex mounting among female Japanese macaques occurred most frequently during the follicular and periovulatory phases of the cycle, and not at all during the luteal phase, paralleling the pattern found in heterosexual mounting behavior. These findings suggest a link between hormonal fluctuations and patterns of sexual mounting, regardless of whether the partner is of the same or opposite sex.     

Behavioral and adrenocortical responses of rhesus macaque mothers to infant separation in an unfamiliar environment

The behavioral and adrenocortical responses of rhesus macaque mothers to a series of four consecutive 4-day separations from their 5-month old infants in an unfamiliar environment were examined. A biphasic behavioral response to separation was observed, with passive behavior, locomotion, and vocalization highest on Day 1 of separation, and self-directed behaviors and environmental exploration peaking during Days 2–4. Stereotyped locomotion increased, and passive behavior decreased, across successive weeks of separation. The rhesus mothers exhibited substantial cortisol elevations one and two hours postseparation, with cortisol decreasing on the fourth day of separation. The cortisol response was strongest during the first week of separation, but robust elevations occurred in response to repeated separations. No signs of behavioral depression were observed. The results indicate that infant separation combined with removal to a novel environment can be a potent stressor for rhesus macaque mothers.     

Use of assisted reproductive technologies in the propagation of rhesus macaque offspring

The assisted reproductive technologies (ARTs) as tailored to the production of rhesus monkeys at the Oregon National Primate Research Center (ONPRC) are described. Efficient fertilization of mature oocytes recovered by aspiration from females subjected to follicular stimulation was achieved with fresh or frozen sperm by intracytoplasmic sperm injection (ICSI). Embryo development to the early cleavage stage occurred at high frequency. Cryopreserved embryos showed high postthaw survival and were also transferred in efforts to establish pregnancies. Three methods of transfer were evaluated, two involving embryo placement into the oviduct, laparoscopy and minilaparotomy, and a nonsurgical, transcervical approach that resulted in uterine deposition. Early cleaving embryos (Days 1-4) were transferred into the oviducts of synchronized recipients with optimal results and pregnancy rates of up to 36%. Pregnancy rates were similar when two fresh or frozen embryos were transferred (28- 30%), although more than two embryos had to be thawed to compensate for embryo loss during freeze-thawing. Normal gestational lengths, birth weights, and growth curves were seen with ART-produced infants compared with infants produced by natural mating in the timed mated breeding (TMB) colony at the ONPRC. In 72 singleton pregnancies established following the transfer of ART-produced embryos, the live-birth rate, at 87.5%, was statistically identical to that for the TMB colony. Further development of the ARTs should result in increasing use of these techniques to augment conventional approaches to propagating monkeys, especially those of defined genotypes.     

The adaptive value of humor and laughter

Most explanations for humor neglect important types of humor, such as tickling and word play; or raise difficult evolutionary theoretical problems, such as group selection, dubious fitness benefits, and excessive complexity of design; or ignore the data on humor and laughter. The present theory was based on the following observations. Tickling entails a mock attack at vulnerable body spots, and may provide youngsters with practice in defending themselves. The child's laughter is pleasant and encourages the tickler to persist. Similarly, juvenile primates including children encourage roughhousing by laughter and other emotional expressions. We also laugh at humorous content that provides striking counter-examples (incongruities), as in word play, or that informs us about fitness-relevant topics such as sexual, aggressive, and social poise scenarios. The present theory is that the pleasure of humor motivates us to seek out poignant, fitness- enhancing input of this sort. Laughter evolved to allow us to continue to recieve amusement. Laughter is a pleasant social signal that prompts the humorist to persist in providing this edifying stimulation. In response to true wit, laughter conveys appreciation and gratitude—an intention to reciprocate for having received a stimulating idea. Thus, humor benefits both humorist and laughter. This theory and others are evaluated in the light of evolutionary principles and relevant data.     

Selfish mothers: reproductive expenditure and resource availability in bighorn ewes

We present a marginal value model explaining intraspecific andinterspecific variation of mating systems in nonterritorialungulates. The model takes into account the simultaneous effectsof spatial and temporal distribution of females, female groupsize, male-male competition, female choice, and the operationalsex ratio (i.e., the proportion of estrous females). The modelpredicts that higher numbers of females per group increasesthe average exploitation time of such groups by males. An increasein female group density, operational sex ratio, and age-specificfighting success of males are predicted to reduce the averageexploitation time of female groups, leading to roving of males(i.e., moving between female groups). In contrast, an increasein die female rejection rate of males and in the time spentby males on nonmating activities (i. e., foraging, lying down,ruminating, migrating) are predicted to increase the averageexploitation time of female groups and to favor staying behaviorof males (i.e., defending a female group over a longer periodof time). Consequently, die model predicts that young maleswill tend to be "stayers," whereas middle-aged and old malesare expected to be "rovers." Model predictions were tested widifield data collected on muskoxen Ovibos moschatus in a naturalpopulation in west Greenland. Observed correlations betweenbull exploitation times of cow groups and the six above-mentionedsocial and environmental parameters were all in die predicteddirection and statistically significant in five of die six cases.Overall, 69% of die observed variation in exploitation timeof cow groups by males was explained by die model predictions.Stepwise regression suggested that, of die six parameters, variationin sex ratio (R² = .56) and time spent on nonmating activities(R² = .35) had the largest effects on male exploitation time.Also, die observed age-specific variation in bull exploitationtime of cow groups was as predicted.     

Radio tracking of a male Japanese macaque emigrated from its group

A male Japanese macaque's ranging behavior before and after emigration from its group was investigated by using radiotelemetry techniques. The male's locations before leaving the troop were regarded as those of the troop, while those after leaving were regarded as those of a solitary male. Monthly home range sizes of the male with the troop were larger than those of the male moving alone, while the whole home range of the male with the troop for three months was much smaller than that of the male moving alone for five months. Overlaps between the male's home ranges with the troop between months were much greater than those between the ranges of the male moving alone. One neighboring troop's home range overlapped the male's range in August and September, and another neighboring troop's range overlapped the male's in October. The mean travel distance and speed of the male with the troop per day did not differ significantly from those of the male moving alone. The results suggest that emigrated males of Japanese macaques may visit home ranges of some troops and stay for a while without interacting troop monkeys before they decide to visit or join the troops.     

Morphological changes of female reproductive organs of Japanese monkeys with reproductive conditions

Macroscopic and histological changes were examined on the female reproductive organs of Japanese monkeys (Macaca fuscata) with varying reproductive status in enclosed and provisioned troops. The weight and size of reproductive organs are described. The size of uterus declined in 2–3 months after parturition. The number of parturition was roughly estimated by degrees of sclerosis in myometrial vessels. The nipple length of parous animals was longer than that of nulliparous ones. The bilateral difference in the length (more than 3 mm) between nipples indicated the experience of nursing. Interpreting ovaries on the basis of macroscopic examination alone was less precise. The present results suggested that the female sexual maturity and the experience of nursing can be estimated by the measurement of reproductive organs in the Japanese monkey.     

Neural correlates of social target value in macaque parietal cortex

Animals as diverse as arthropods [1], fish [2], reptiles [3], birds [4], and mammals, including primates [5], depend on visually acquired information about conspecifics for survival and reproduction. For example, mate localization often relies on vision [6], and visual cues frequently advertise sexual receptivity or phenotypic quality [5]. Moreover, recognizing previously encountered competitors or individuals with preestablished territories [7] or dominance status [1, 5] can eliminate the need for confrontation and the associated energetic expense and risk for injury. Furthermore, primates, including humans, tend to look toward conspecifics and objects of their attention [8, 9], and male monkeys will forego juice rewards to view images of high-ranking males and female genitalia [10]. Despite these observations, we know little about how the brain evaluates social information or uses this appraisal to guide behavior. Here, we show that neurons in the primate lateral intraparietal area (LIP), a cortical area previously linked to attention and saccade planning [11, 12], signal the value of social information when this assessment influences orienting decisions. In contrast, social expectations had no impact on LIP neuron activity when monkeys were not required to make a choice. These results demonstrate for the first time that parietal cortex carries abstract, modality-independent target value signals that inform the choice of where to look.