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Studies in multiple host species have shown that gut microbial diversity and composition change during pregnancy and lactation. However, the specific mechanisms underlying these shifts are not well understood. Here, we use longitudinal data from wild Phayre's leaf monkeys to test the hypothesis that fluctuations in reproductive hormone concentrations contribute to gut microbial shifts during pregnancy. We described the microbial taxonomic composition of 91 fecal samples from 15 females (n = 16 cycling, n = 36 pregnant, n = 39 lactating) using 16S rRNA gene amplicon sequencing and assessed whether the resulting data were better explained by overall reproductive stage or by fecal estrogen (fE) and progesterone (fP) concentrations. Our results indicate that while overall reproductive stage affected gut microbiome composition, the observed patterns were driven by reproductive hormones. Females had lower gut microbial diversity during pregnancy and fP concentrations were negatively correlated with diversity. Additionally, fP concentrations predicted both unweighted and weighted UniFrac distances, while reproductive state only predicted unweighted UniFrac distances. Seasonality (rainfall and periods of phytoprogestin consumption) additionally influenced gut microbial diversity and composition. Our results indicate that reproductive hormones, specifically progestagens, contribute to the shifts in the gut microbiome during pregnancy and lactation.

In species with strong male-male competition, access to females in multimale-multifemale groups is usually regulated via a dominance hierarchy. The highest ranking (alpha) male often has priority of access and sires most offspring. The alpha male can change in three basic ways: (i) a recent immigrant or a resident challenges and becomes the new alpha; (ii) formation of a new group; (iii) succession-becoming alpha after higher ranking males have left. When, in a given primate population, the alpha male changes in different ways, two questions arise: (a) which is the most successful tactic and (b) do male attributes, such as age, aggressiveness or propensity to commit infanticide, affect the outcome? We examined these questions in the seasonally breeding Nepal gray langurs (Semnopithecus schistaceus) at Ramnagar, where new alpha males were either recent immigrants or residents. Success was measured as alpha tenure, residency duration, and the number of offspring sired (paternity exclusion based on DNA analysis, 28 infants). We documented 12 alpha-male tenures across two multimale-multifemale groups between 1991 and 1997. The predominant mode of change was the immigrant tactic. Age had no effect perhaps because alpha males were among the youngest adult males in their group. As expected, infanticidal males performed similarly to non-infanticidal ones. Alpha tenure was highly variable and longer for immigrant alphas and hyper-aggressive ones. However, none of the tactics or attributes examined resulted in significantly longer residencies or more offspring, likely because of the timing of immigrations and stochastic effects (i.e., the number of conceptions occurring per alpha tenure). The influence of female mate choice on male reproductive success requires further investigation. Furthermore, it remains to be examined why resident alpha males-with their presumed better knowledge of their opponents -performed so poorly. Am. J. Primatol. 79:e22437, 2017. © 2015 Wiley Periodicals, Inc., (© 2015 Wiley Periodicals, Inc.)

In most group-living mammals, reproductive success declines with increasing age and increases with increasing rank. Such effects have mainly been studied in matrilineal and in "age positive" hierarchies, which are stable and in which high ranking females often outperform low ranking ones. These relationships are less well-understood in age-inversed dominance hierarchies, in which a female's rank changes over time. We analyzed demographic data of 2 wild, unprovisioned groups of gray langurs (Semnopithecus schistaceus) near Ramnagar, Nepal covering periods of 5 years each. Female rank was unstable and age-inversed. We measured reproductive success via birth rates (57 births), infant survival (proportion of infants surviving to 2 years) and number of offspring surviving to 2 years of age (successful births) for 3 age and 3 rank classes. We found that old females performed significantly worse than expected (birth rate P = 0.04; successful births P = 0.03). The same was true for low ranking females (P = 0.04, and P < 0.01, respectively). Infant survival was highest for young and middle-aged as well as for high and middle ranking females. Overall, the results for these unstable hierarchies were rather similar to those for stable hierarchies of other mammals, particularly several nonhuman primates. Compared to a provisioned population of a closely related species, the wild and unprovisioned population examined (i) showed stronger age effects, while (ii) female reproductive success was equally affected by rank. Future comparative studies are needed to examine whether captive or provisioned populations deviate predictably from wild populations., (© 2016 International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd.)

An accurate description of reproductive characteristics and ovarian endocrinology is necessary to address questions about the reproductive strategies and life history of a species and for meaningful, cross species analyses. Here we used analysis of fecal estradiol (fE) and behavioral observations to determine for the first time the reproductive characteristics and endocrinology of a wild group (N = 18 adult and 3 adolescent females) of Sanje mangabeys (Cercocebus sanjei). The study was conducted in the Udzungwa Mountains National Park, Tanzania, from October 2008 through September 2010. Average cycle length (±SD) was 29.3 ± 3.2 days in adults and 51.4 ± 5.5 days in adolescents. Menses appeared within 5.1 ± 2.1 days in adults and 4.8 ± 0.3 days in adolescents after the end of maximum tumescence, and lasted 6.7 ± 3.1 and 10.3 ± 5.0 days, respectively. Infant death tended to reduce the number of cycles to conception (4.3 ± 1.5 cycles after a surviving infant vs. 2.6 ± 1.0 cycles after infant death). Adolescents cycled for at least 16 months without conceiving. Implantation bleeding began 17.5 ± 0.7 days from the onset of detumescence, and lasted 10.0 ± 1.4 days. Gestation length averaged 171.8 ± 3.4 days. Postpartum amenorrhea lasted 6.7 ± 2.3 months while females whose infants had died resumed cycling within 14.3 ± 5.9 days. The interbirth interval after a surviving infant averaged 20.0 ± 4.3 months. These reproductive characteristics of the Sanje mangabey resembled those of other mangabeys and related cercopithecines, with the exception of an earlier onset and longer duration of menstruation and implantation bleeding. Further information on the physiology of the Sanje mangabey is needed to clarify what factors may cause the unusual characteristics of both, their menses and implantation bleeding., (© 2014 Wiley Periodicals, Inc.)

Female reproduction is known to be influenced by food availability and its impact on energetic status. However, emerging evidence suggests that the phytochemical content of food may also be an important factor. Here, we investigated this hypothesis, presenting 20 months of data on fecal progestin (fP) patterns in wild female Phayre's leaf monkeys (Trachypithecus phayrei crepusculus). We examined whether (a) the availability of Vitex (a plant known to contain phytochemicals) might be linked to seasonal fP levels, (b) fP levels were associated with female reproductive performance, and (c) reproductive performance might also be linked with energetic status (as measured by physical condition). We collected fecal samples (N=2077) from 10 adult females to analyze estrogen (fE) and progestin (fP) metabolites, behavioral data from 7 cycling females to determine receptivity, and monthly data on Vitex availability and female physical condition. Seasonally elevated fP levels were found in all females, with higher levels when Vitex leaves and fruits were abundant. During the period of high progestins, females had longer cycle lengths and follicular phases, while receptive periods did not change. Nevertheless, when ovulations occurred, females were more likely to conceive. On the other hand, conceptions were also more likely when physical condition was improving, suggesting that the effects of phytochemicals and energetic status on reproduction may be difficult to separate. Although our results support the predicted effects of Vitex on endocrine and reproductive function, future studies with detailed feeding data and chemical analyses of plants are needed to confirm this finding., (Copyright © 2010 Elsevier Inc. All rights reserved.)

Understanding female reproductive characteristics is important for assessing fertility, interpreting female behavior, and designing appropriate conservation and captive management plans. In primate species lacking morphological signs of receptivity, such as most colobines, determination of reproductive parameters depends on the analysis of reproductive hormones. Here, we use fecal hormone analysis to characterize cycle patterns (N=6 females) and gestation length (N=7 females) in a group of wild Phayre's leaf monkeys (Trachypithecus phayrei crepusculus) in Phu Khieo Wildlife Sanctuary, Thailand. We found that both fecal estrogen (fE) and progestin (fP) levels showed clear biological patterns indicative of ovulation and conception. However, because fP patterns were inadequate in determining the end of the luteal phase, we used fE rather than fP patterns to delineate menstrual cycle parameters. We found a mean cycle length of 28.4 days (N=10), with follicular and luteal phases of 15.4 (N=10) and 12.5 days (N=14), respectively. On average, females underwent 3.57 (N=7) cycles until conception. Average gestation length was 205.3 days (N=7), with fE levels increasing over the course of pregnancy. Overall, the reproductive characteristics found for Phayre's leaf monkeys were consistent with results for other colobine species, suggesting that fecal hormone monitoring, particularly for fE metabolites, can provide useful reproductive information for this species., (© 2010 Wiley-Liss, Inc.)

Within phylogenetic limits reproductive characteristics of a given species may vary between populations in response to ecological and social factors. For instance, in environments where high quality nutrition is readily available, the onset and speed of reproduction are often accelerated. Other influencing factors might be maternal experience or the sex of the infant. Here we present data on reproductive characteristics for the silvered leaf monkey (Trachypithecus cristatus), a medium-sized Asian colobine housed at the Wildlife Conservation Society's Bronx Zoo as a one-male group. To place the species into an appropriate phylogenetic context, we limited our comparison to other colobine species. Demographic data span 21.4 years (October 1985 to March 2007) and derive from 30 adult females (128.0 female years). Detailed behavioral data stem from a 2.2 years study (November 2002 to January 2005; 734 days, 4,225 hr). As in other Asian colobines, receptive periods were short (mean=4.3 days, n=68). This is expected for one-male groups where receptivity likely indicates, rather than conceals, ovulation. Gestation length was estimated based on a change in the pattern of sexual behavior (mean=194.6 days, n=7). It fell within the range reported for the taxon. Births occurred year round, at an early age (mean=2.9 years, n=8), at short intervals (mean=14.9 months, n=59) in combination with a short lactation (mean 12.1 months, n=9) likely due to the nearly unlimited availability of nutrition in this zoo setting. Primiparous females tended to have a longer first interbirth interval but infant survival rates were similar to multipara possibly due to the absence of predators. Maternal investment was independent of the infant's sex and birth sex ratio was even. Our results emphasize that when interpreted with caution, zoo populations yield realistic reproductive characteristics that can help fill the gap in our knowledge about colobine life history.

Data from four Asian colobine populations, wild (Ramnagar) and provisioned (Jodhpur) Hanuman langurs, wild Phayre's leaf monkeys (Phu Khieo Wildlife Sanctuary), and captive silvered langurs (Wildlife Conservation Society's Bronx Zoo) were analyzed with respect to reproductive and behavioral trends of aging. All but one female (from a total of seven) became menopausal 1.8 to 5+ years prior to death with a lag time between last parturition and death ranging from 3.0 to 9.0 years (n=8). Hormonal analysis revealed constantly low and acyclic levels of immunoreactive pregnanediol-3-glucuronide (iPdG) in one old, wild female supporting the notion of true menopause. Nonsexual behavior was analyzed based on quantitative data collected for 6 old and 26 younger, adult females simultaneously (1,378.5 h). No support was found for social disengagement, but old females were more inactive and spent less time feeding. Altogether the data support earlier claims of menopause and extended postreproductive life spans in colobine monkeys. Future behavioral studies should aim at longitudinal assessments of behavioral changes and incorporate energetic data as well as testing of social continuity and selectivity.

In species with a high risk of infanticide, a conflict of interest exists between the sexes over the amount of paternity information that is available to males. While females are expected to keep males unaware of their reproductive status in order to confuse paternity, selection should favor those male traits that enhance the males' assessment of female status and consequently of paternity probability. In Hanuman langurs (Semnopithecus entellus), a species that is extremely vulnerable to infanticide, females have been shown to successfully conceal the exact timing of ovulation from males--perhaps because they exhibit no sexual swelling and mate during all reproductive phases, including gestation. Nevertheless, it remains unclear whether males have hitherto unrecognized information about females' reproductive condition on a broader level that could still enhance male reproductive success. We investigated male assessment of female reproductive states in a population of wild Hanuman langurs as indicated by changes in male behavior, such as rates of copulations, anogenital inspections, and consortships, in relation to different female receptive periods (pregnant, fertile-nonconceptional, and conceptional). Our data indicate that males were able to discern qualitatively distinct reproductive states. Males were more interested in fertile than pregnant females, as indicated by higher copulation rates. Based on consortships, males distinguished fertile from nonfertile phases, as well as fertile, nonconceptional receptive periods from conceptional ones. Hanuman langur males are thus not as unaware of female reproductive condition as previously thought, supporting the idea of an ongoing battle of the sexes over paternity information. However, granting some knowledge while at the same time concealing the exact day of ovulation may also reflect a pure female strategy of balancing paternity concentration with paternity confusion, which is the most likely strategy in this system with high infanticide risk and male defense of infants., ((c) 2005 Wiley-Liss, Inc.)

The time spent between sleeping periods, which is called the active period, has to accommodate all essential activities, including feeding, resting, social behavior, and reproduction. To minimize costs in terms of, e.g., predation risk, suboptimal foraging, or sleep deficiency, the active period of diurnal animals should be less than or equal to the daylight period. Thus, the active period of an animal should be shaped by local environmental conditions as well as by metabolic and reproductive demands. Chimpanzees, which exhibit reduced predator pressure and a flexible fission-fusion society, were chosen as a model to explore these links. We investigated the influence of sex, female reproductive status, dominance rank, and season on the duration of the active period of adult chimpanzees at Gombe National Park, Tanzania (1975-1992). Sexually nonreceptive females had shorter active periods compared to males, while receptive females had even longer active periods than males. Dominance rank did not influence the duration of the active period of nonreceptive females, but high- and middle-ranking males had shorter active periods compared to low-ranking males. Nonreceptive females exhibited longer active periods during the dry season than in the wet season. No seasonal effect was discovered for males, perhaps because they already had long active periods in the wet season. Nonreceptive females seem to be able to accommodate all essential activities in the daylight period available, probably because they live less socially than males. Thus, the active period does not reflect differences in female competitive abilities, but does reflect such differences in males. The duration of the active period appears to be a simple, reliable tool for exploring basic responses and constraints in animal societies.

Life history variables such as the age at first reproduction and the interval between consecutive births are measures of investment in growth and reproduction in a particular population or species. As such they allow for meaningful comparisons of the speed of growth and reproduction between species and between larger taxa. Especially in primates such life history research has far reaching implications and has led for instance to the “grandmother hypothesis”. Other links have been proposed with respect to dietary adaptations: Because protein is essential for growth and one of the primary sources of protein, leaves, occurs much less seasonally than fruits, it has been predicted that folivorous primates should grow faster compared to frugivorous ones. However, when comparing folivorous Asian colobines with frugivorous Asian macaques we recently documented a longer, instead of a shorter gestation length in folivores while age at first reproduction and interbirth interval did not differ. This supports earlier findings for Malagasy lemurs in which all life history variables tested were significantly longer in folivores compared to frugivores. Wondering why these trends were not apparent sooner, we tried to reconstruct our results for Asian primates with data from four popular life history compilations. However, this attempt failed; even the basic, allometric relationship with adult female body mass that is typical for life history variables could not be recovered. This negative result hints at severe problems with data quality. Here we show that data quality can be improved significantly by standardizing the variables and by controlling for factors such as nutritional conditions or infant mortality. Ideally, in the future, revised primate life history data should be collated in a central database accessible to everybody. In the long run such an initiative should be expanded to include all mammalian species. [ABSTRACT FROM AUTHOR]

Extended sexual receptivity in primates is thought to facilitate paternity confusion, thus decreasing the risk of infanticide. However, females might also provide some indication of ovulation to attract preferred males during fertile periods. We examined female mate preferences across defined receptive periods ( N = 59) in a group of wild Phayre's leaf monkeys ( Trachypithecus phayrei crepusculus) at Phu Khieo Wildlife Sanctuary (February-September 2006; 2,603 contact hours). The group contained seven cycling adult females and three reproductively active males (one adult and two adolescents). We predicted that females would prefer the adult male during periovulatory ( POP) receptive periods, but the adolescent males during nonperiovulatory ( NPOP) and postconceptive ( PC) periods. We collected focal and ad libitum data on sexual and agonistic behaviors to determine female preferences and male awareness of female fertility. We also determined the degree of mating overlap to assess if males were capable of monopolizing females. Our results indicate that females were more frequently proceptive and receptive toward the adult male during POP. By contrast, females were more proceptive and receptive toward one of the adolescent males during PC periods, but rarely interacted with the other adolescent. Patterns of attractivity and agonism across receptive periods suggested that the adult male could detect fertility, while the preferred adolescent could not. Finally, we found a high degree of overlap in total receptive period days, but a low degree of overlap in POP receptive days, suggesting that the adult male might have monopolized females, especially since he seemed to be aware of female fertility. Although these results suggest that females provide some information on ovulation, they also suggest that females attempt to confuse paternity, perhaps capitalizing on male differences in the ability to detect fertility. Am. J. Primatol. 74:471-481, 2012. © 2012 Wiley Periodicals, Inc. [ABSTRACT FROM AUTHOR]

Understanding female reproductive characteristics is important for assessing fertility, interpreting female behavior, and designing appropriate conservation and captive management plans. In primate species lacking morphological signs of receptivity, such as most colobines, determination of reproductive parameters depends on the analysis of reproductive hormones. Here, we use fecal hormone analysis to characterize cycle patterns ( N=6 females) and gestation length ( N=7 females) in a group of wild Phayre's leaf monkeys ( Trachypithecus phayrei crepusculus) in Phu Khieo Wildlife Sanctuary, Thailand. We found that both fecal estrogen (fE) and progestin (fP) levels showed clear biological patterns indicative of ovulation and conception. However, because fP patterns were inadequate in determining the end of the luteal phase, we used fE rather than fP patterns to delineate menstrual cycle parameters. We found a mean cycle length of 28.4 days ( N=10), with follicular and luteal phases of 15.4 ( N=10) and 12.5 days ( N=14), respectively. On average, females underwent 3.57 ( N=7) cycles until conception. Average gestation length was 205.3 days ( N=7), with fE levels increasing over the course of pregnancy. Overall, the reproductive characteristics found for Phayre's leaf monkeys were consistent with results for other colobine species, suggesting that fecal hormone monitoring, particularly for fE metabolites, can provide useful reproductive information for this species. Am. J. Primatol. 72:1073-1081, 2010. © 2010 Wiley-Liss, Inc. [ABSTRACT FROM AUTHOR]

In polygynous, sexual dimorphic species with higher variance in male reproductive success compared with females, females are expected to invest more heavily in sons than daughters within the constraints imposed by their physical condition ( Science 1973; 179:90). Mothers in good condition, usually those of high rank, should produce more sons than females in poor condition or of low rank. We investigated sex allocation and sex-biased maternal investment in a population of wild Hanuman langurs using rank and group size as approximations of female physical condition. Our results show that reproductive costs of sons were higher with both significantly longer interbirth intervals following male births and longer lactational periods for sons. Not in all groups did analyses of rank-dependent sex allocation reveal the expected pattern of high-ranking mothers producing more sons. However, sex ratio was significantly influenced by group size, with females from larger groups, i.e., in worse physical condition, producing a daughter-biased sex ratio. In fact, only females of population-wide superior physical condition can be expected to produce sons, because in Hanuman langurs males disperse and compete population-wide. Thus, our results support the Trivers–Willard model and may explain the mixed evidence accruing from studies of single groups. We present a graphical model of how group size and dominance-related differences in energy gain may influence sex allocation under different competitive regimes relative to overall resource availability. Tests of adaptive sex allocation models should consider whether reproductive competition of the preferred sex takes place primarily within a group or within the population. [ABSTRACT FROM AUTHOR]

Reproductive parameters and sexual behavior of free-ranging Hanuman langurs (Presbytis entellus) were studied over a 13-year period at Jodhpur, India in a population that breeds throughout the year. Long-term monitoring of individually identified females living in one-male-multi-female troops revealed a mean cycle length of 24.1 days (n = 113), a mean gestation of 200.3 days (n = 31), menarche at 29.0 months (n = 10), first conception at 35.0 months (n=12), arid a mean birth interval of 16.7 months (n = 114). The loss of unweaned infants accelerated the resumption of menstruation, receptivity, and attractivity; shortened the period between estrus and next conception; and reduced the median birth interval by 20.5%, thus supporting the sexual selection hypothesis of male infanticide. The decline of fertility with age (as measured by the rates of conception per estrus period), a regular post reproductive survival for up to 9 years (which can account for about 25% of a female's Life span) and indications for the existence of a "true menopause" support the view that a post reproductive period in Langurs is the result of natural selection. There is very limited evidence for situation-dependent receptivity, because only 7.5% of all estrous days (n = 1,037) fell outside of the mid-cycle period with at the same time strongly reduced proceptivity and attractivity. Moreover, posteonception estrus behavior showed a stereotypical pattern during 31 pregnancies and did not reflect a situation-dependent response to the immigration of new and potentially infanticidal males. It is likely that females competed for sperm of the harem holder, because the probability of conception increased significantly with an increase in the number of copulations, and when the number of females copulating on the same day decreased. [ABSTRACT FROM AUTHOR]