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1.  Pregnancy weight gain: marmoset and tamarin dads show it too 
Biology letters  2006;2(2):181-183.
Paternal behaviour is critical for the survival of offspring in many monogamous species. Common marmoset (Callithrix jacchus) and cotton-top tamarin (Saguinus oedipus) fathers spend as much or more time caring for infants than mothers. Expectant males of both species showed significant increases in weight across the pregnancy whereas control males did not (five consecutive months for marmoset males and six months for cotton-top tamarin males). Expectant fathers might be preparing for the energetic cost of fatherhood by gaining weight during their mate’s pregnancy.
PMCID: PMC1483903  PMID: 16810338
weight gain; paternal care; couvades; primates
2.  Social Effects via Olfactory Sensory Stimuli on Reproductive Function and Dysfunction in Cooperative Breeding Marmosets and Tamarins 
American journal of primatology  2012;75(3):202-211.
Most primates are social species whose reproduction is influenced by their social relationships. The cotton-top tamarin, Saguinus oedipus, and the common marmoset, Callithrix jacchus, are cooperative breeding species where the family structure alters reproductive function in many ways. While primates receive social effects on reproduction via all sensory stimuli, the marmosets and tamarins are particularly influenced by olfactory/chemosensory stimuli. The olfactory sensory processing is the ‘social glue’ that keeps the family together.
This review describes a number of studies using the marmosets and tamarins at the University of Wisconsin to demonstrate how odor cues are used for altering reproductive function and dysfunction. Several key studies will be discussed to show the role of odor signaling of the female reproductive state. The suppressive effects of odors are mediated by priming odors and can cause a suppressive influence on ovulation in young females via their mother’s scents. Additionally, odor cues from the infant function as priming odors to ensure that fathers and mothers are present and receptive to their parental care duties. Neural pathways occur via the processing of priming odors that consequently stimulate alterations in the behavioral and endocrine response to the stimuli. The dynamics of the cooperative breeding system ensure that offspring have essential needs met and that they develop in a family environment. Olfactory communication plays a key role in maintenance of the social system of Callitrichid monkeys.
PMCID: PMC3502670  PMID: 22890774
3.  The ecology and evolution of patience in two New World monkeys 
Biology Letters  2005;1(2):223-226.
Decision making often involves choosing between small, short-term rewards and large, long-term rewards. All animals, humans included, discount future rewards—the present value of delayed rewards is viewed as less than the value of immediate rewards. Despite its ubiquity, there exists considerable but unexplained variation between species in their capacity to wait for rewards—that is, to exert patience or self-control. Using two closely related primates—common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus)—we uncover a variable that may explain differences in how species discount future rewards. Both species faced a self-control paradigm in which individuals chose between taking an immediate small reward and waiting a variable amount of time for a large reward. Under these conditions, marmosets waited significantly longer for food than tamarins. This difference cannot be explained by life history, social behaviour or brain size. It can, however, be explained by feeding ecology: marmosets rely on gum, a food product acquired by waiting for exudate to flow from trees, whereas tamarins feed on insects, a food product requiring impulsive action. Foraging ecology, therefore, may provide a selective pressure for the evolution of self-control.
PMCID: PMC1626214  PMID: 17148172
temporal discounting; impulsivity; rate maximization; tamarins; marmosets
4.  Nononcogenic deletion mutants of herpesvirus saimiri are defective for in vitro immortalization. 
Journal of Virology  1986;57(2):701-705.
Herpesvirus saimiri L-DNA sequences between 0.0 and 4.0 map units (4.5 kilobase pairs) are required for oncogenicity; these sequences are not required for replication of the virus. To investigate the basis for the lack of oncogenicity of mutants with deletions in this region and to study the function of this region, we developed a reliable system for in vitro immortalization by herpesvirus saimiri. In contrast to peripheral blood lymphocytes from cotton-top tamarins (Saguinus oedipus) and owl monkeys (Aotus sp.), infection of peripheral blood lymphocytes from common marmosets (Callithrix jacchus) in vitro with herpesvirus saimiri consistently yielded continuously growing lymphoblastoid cell lines. Such cell lines were established using strains of herpesvirus saimiri from group A and group non-A, non-B; however, repeated attempts to immortalize common marmoset peripheral blood lymphocytes using strains from group B were not successful. Common marmoset cell lines immortalized by herpesvirus saimiri were T12+, T8+, T4-, and B1-, indicating that they were derived from suppressor/cytotoxic T lymphocytes. Cell lines could not be established using the nononcogenic mutants 11att and S4, both of which were derived from the group A strain 11 virus. Strain 11att has a spontaneous deletion and S4 has a constructed deletion in the 0.0 to 4.0 map unit region. Constructed strains which had these deleted sequences restored did immortalize common marmoset peripheral blood lymphocytes. Thus, the nononcogenic deletion mutants are defective for immortalization. This system should facilitate attempts to define the sequences responsible for immortalization and to determine their function.
PMCID: PMC252789  PMID: 3003401
5.  Neonatal and Pubertal Development in Males of a Cooperatively Breeding Primate, the Cotton-Top Tamarin (Saguinus oedipus oedipus)1 
Biology of reproduction  2002;66(2):282-290.
In cooperatively breeding groups of mammals, reproduction is usually restricted to a small number of individuals within the social group. Sexual development of mammals can be affected by social environment, but we know little regarding effects of the cooperative-breeding system on males. Cotton-top tamarin (Saguinus oedipus oedipus) offspring typically do not reproduce in their natal group, even though they may be physically mature. We examined neonatal and pubertal development in captive male cotton-top tamarins as an example of reproductive development within a cooperative-breeding system and to compare cotton-top tamarins with the general primate model. Puberty was characterized using both hormonal and physical measures. Data were collected on urinary levels of LH, testosterone (T), dihydrotestosterone (DHT), cortisol, and the ratio of DHT to T; testicular development; body weight; and breeding age. We determined that 1) pubertal LH secretion began at Week 37, 2) a surge of T secretion followed at Weeks 41–44, and 3) an increase in the metabolism of T to DHT may have occurred at an average age of 48.6 wk. Most of the rapid weight gain was completed by Week 24, before hormonal increases and rapid scrotal growth. We concluded that rapid pubertal testicular growth in captive cotton-top males was completed by an average 76 wk, but that completion of the individual pubertal spurt can occur between 56 and 122 wk. In a cooperative-breeding system, the opportunity for successful reproduction is dictated by the social environment, but we found no evidence that male offspring were developmentally suppressed in their natal social groups. Our findings suggest that puberty in male New World callitrichid primates occurs more quickly than puberty in Old World primates, even though both have similar patterns of development.
PMCID: PMC1482832  PMID: 11804940
developmental biology; luteinizing hormone; puberty; steroid hormones; testis
6.  Variation in Oxytocin is Related to Variation in Affiliative Behavior in Monogamous, Pairbonded Tamarins 
Hormones and behavior  2010;58(4):614-618.
Oxytocin plays an important role in monogamous pairbonded female voles, but not in polygamous voles. Here we examined a socially-monogamous cooperatively breeding primate where both sexes share in parental care and territory defense for within species variation in behavior and female and male oxytocin levels in 14 pairs of cotton-top tamarins (Saguinus oedipus), In order to obtain a stable chronic assessment of hormones and behavior, we observed behavior and collected urinary hormonal samples across the tamarins’ three week ovulatory cycle. We found similar levels of urinary oxytocin in both sexes. However, basal urinary oxytocin levels varied ten-fold across pairs and pair-mates displayed similar oxytocin levels. Affiliative behavior (contact, grooming, sex) also varied greatly across the sample and explained more than half the variance in pair oxytocin levels. The variables accounting for variation in oxytocin levels differed by sex. Mutual contact and grooming explained most of the variance in female oxytocin levels whereas sexual behavior explained most of the variance in male oxytocin levels. The initiation of contact by males and solicitation of sex by females were related to increased levels of oxytocin in both. This study demonstrates within-species variation in oxytocin that is directly related to levels of affiliative and sexual behavior. However, different behavioral mechanisms influence oxytocin levels in males and females and a strong pair relationship (as indexed by high levels of oxytocin) may require the activation of appropriate mechanisms for both sexes.
PMCID: PMC2933949  PMID: 20600045
Oxytocin; affiliative behavior; cotton-top tamarins; monogamy; cooperative breeding; sex differences
7.  Cooperative breeders do cooperate 
Behavioural processes  2007;76(2):138-141.
Bergmüller et al. (2007) make an important contribution to studies of cooperative breeding and provide a theoretical basis for linking the evolution of cooperative breeding with cooperative behavior. We have long been involved in empirical research on the only family of nonhuman primates to exhibit cooperative breeding, the Callitrichidae, which includes marmosets and tamarins, with studies in both field and captive contexts. In this paper we expand on three themes from Bergmüller et al. (2007) with empirical data. First we provide data in support of the importance of helpers and the specific benefits that helpers can gain in terms of fitness. Second, we suggest that mechanisms of rewarding helpers are more common and more effective in maintaining cooperative breeding than punishments. Third, we present a summary of our own research on cooperative behavior in cotton-top tamarins (Saguinus oedipus) where we find greater success in cooperative problem solving than has been reported for non-cooperatively breeding species.
PMCID: PMC2080785  PMID: 17703900
8.  Lack of Adaptation of Chimeric GB Virus B/Hepatitis C Virus in the Marmoset Model: Possible Effects of Bottleneck ▿  
Journal of Virology  2009;83(16):8062-8075.
Approximately 3% of the world population is chronically infected with hepatitis C virus (HCV). GB virus B (GBV-B), a surrogate model for HCV, causes hepatitis in tamarins and is the virus phylogenetically most closely related to HCV. Previously we described a chimeric GBV-B containing an HCV insert from the 5′ noncoding region (NCR) that was adapted for efficient replication in tamarins (Saguinus species). We have also demonstrated that wild-type (WT) GBV-B rapidly adapts for efficient replication in a closely related species, the common marmoset (Callithrix jacchus). Here, we demonstrate that the chimeric virus failed to adapt during serial passage in marmosets. The chimeric virus was passaged four times through 24 marmosets. During passage, two marmoset phenotypes were observed: susceptible and partially resistant. Although appearing to adapt in a resistant animal during a prolonged and gradual increase in viremia, the chimeric GBV-B failed to replicate efficiently upon passage to a naïve marmoset. The resistance was specific to the chimeric virus, as the chimeric virus-resistant animals were susceptible to marmoset-adapted WT virus during rechallenge studies. Three isolates of the chimeric virus were sequenced, and 20 nucleotide changes were observed, including eight amino acid changes. Three unique changes were observed in the 5′ NCR chimeric insert, an area that is highly conserved in HCV. We speculate that the failure of the chimeric virus to adapt in marmosets might be due to a bottleneck that occurs at the time of infection of resistant animals, which may lead to a loss of fitness upon serial passage.
PMCID: PMC2715777  PMID: 19474092
9.  Costs of Caregiving: Weight Loss in Captive Adult Male Cotton-Top Tamarins (Saguinus oedipus) Following the Birth of Infants 
We examined changes in weight for 10 captive adult male cotton-top tamarins (Saguinus oedipus) from before the birth of infants through the first 16 weeks of infant life. Compared to before birth, males weighed significantly less in Weeks 1–4, 5–8, and 9–12 following the birth. Weights in Weeks 13–16 did not differ significantly from prebirth weights. Maximum weight loss for individual males ranged from 1.3 to 10.8% of prebirth body weight. Males in groups with fewer helpers lost significantly more weight than ones in groups with more helpers. For the 3 males that had no helper other than their mates, weight loss was particularly striking, ranging from 10.0 to 10.8% of their prebirth body weight. These results suggest that caring for infants is energetically costly, and that in this cooperatively breeding species, the presence of more individuals to share the burden of infant carrying reduces the cost to individual caregivers.
PMCID: PMC1483063  PMID: 16804560
cotton-top tamarin; Saguinus; cooperative breeding; weight loss; infant care
10.  Long-term Memory for Calls of Relatives in Cotton-top Tamarins (Saguinus oedipus) 
Recognition of relatives is important for dispersing animals to avoid inbreeding and possibly for developing cooperative, reciprocal relationships between individuals after dispersal. We demonstrate under controlled captive conditions that cotton-top tamarins (Saguinus oedipus) have a long-term memory for long calls of relatives from which they had been separated for periods ranging from 4 to 55 months. Tamarins responded with lower levels of arousal behavior to playbacks of long calls from current mates and from separated relatives compared to calls of unfamiliar, unrelated tamarins. Four animals had been out of contact with relatives for more than 4 years and still showed recognition as evidenced by low levels of arousal. Results could not be explained in terms of proximity to former relatives. Long-term memory for vocal signatures of relatives is adaptive and may be much more common than has been demonstrated.
PMCID: PMC3191862  PMID: 21574684
cotton-top tamarins; vocalizations; long-term memory; relatives
11.  Differential Hypothalamic Secretion of Neurocrines in Male Common Marmosets: Parental Experience Effects? 
Journal of Neuroendocrinology  2012;24(3):413-421.
Pregnancy and lactation produce a plethora of hormonal changes in females that promote maternal care of offspring. Males in the biparental marmoset species, (Callithrix jacchus), demonstrate high levels of parenting behaviour and express enhanced circulating reproductive hormones. Furthermore, these hormonal changes are influenced by paternal experience. In order to determine if the paternally experienced male marmoset has altered neurocrine hypothalamic release, as the maternal females does, we examined the release of several reproductive neurocrines, dopamine (DA), oxytocin (OT) and vasopressin (AVP) and prolactin (PRL), in cultured explants of the hypothalamus of paternally experienced male marmosets compared with naïve, paternally inexperienced males. DA levels secreted from the isolated hypothalamus were significantly lower in the experienced males while OT and PRL levels were significantly higher than levels found in inexperienced males. PRL levels decreased rapidly in the hypothalamic media suggesting PRL production occurs elsewhere. AVP levels did not change. Stimulation of the cultured explants with oestradiol significantly decreased DA levels in the inexperienced males but did not alter the other neurocrines suggesting a direct effect of oestradiol on DA suppression in the hypothalamus. While other factors such as age and rearing experience with siblings may play a role in hypothalamic neurocrine levels, these results demonstrate that paternal experience may impact the secretion of neurocrines in a male biparental primate.
PMCID: PMC3288632  PMID: 22070606
paternal experience; prolactin; OT; oestradiol; dopamine; vasopressin; hypothalamus
12.  Sexual Communication Between Breeding Male and Female Cotton-Top Tamarins (Saguinus oedipus), and its Relationship to Infant Care 
Male cotton-top tamarins have been shown to be responsive to female scent cues of ovulation, and are known to actively participate in infant care during the time when their mates are fertile. We measured urinary androgen levels and glucocorticoids in seven father tamarins for the first month following the birth of infants to determine 1) whether male tamarins showed an androgen response to their mate’s postpartum ovulation, 2) when androgens rise relative to ovulation, 3) whether there is a glucocorticoid response, and 4) whether males alter their parenting behavior during their mate’s receptive period. All of the males showed a significant increase in urinary androgens prior to the female’s postpartum LH peak, which indicated ovulation. The hormonal increase, which included estradiol, occurred 3–7 days prior to the female’s LH peak at a time that coincided with the female’s follicular period. Corticosterone levels also peaked during that time, but did not correlate with androgen changes. Fathers did not alter their daily infant-carrying patterns relative to the androgen increase or at the time of the mate’s LH peak. We conclude that male cotton-top tamarins experience an increase in androgens that coincides with their mate’s postpartum ovulation, which ensures optimal fertility. However, this sexual communication does not alter father–infant interactions, which already occur at a high rate in this species.
PMCID: PMC1482834  PMID: 15356858
cotton-top tamarin; androgens; glucocorticoids; chemical signaling; ovulation; parenting behavior
13.  Development of a GB Virus B Marmoset Model and Its Validation with a Novel Series of Hepatitis C Virus NS3 Protease Inhibitors†  
Journal of Virology  2004;78(4):2062-2071.
GB virus B (GBV-B), a flavivirus closely related to HCV, has previously been shown to infect and replicate to high titers in tamarins (Saguinus sp.). This study describes the use of GBV-B infection and replication in the common marmoset (Callithrix jacchus) for the successful development and validation of a surrogate animal model for hepatitis C virus (HCV). Infection of marmosets with GBV-B produced a viremia that peaked at 108 to 109 genome copies/ml for a period of 40 to 60 days followed by viral clearance at 60 to 80 days postinfection. Passage of the initial tamarin-derived GBV-B in marmosets produced an infectious stock that gave a more reproducible and consistent infection in the marmoset. Titration of the virus stocks in vivo indicated that they contained 1 infectious unit for every 1,000 genome copies. Cultures of primary marmoset hepatocytes were also successfully infected with GBV-B, with high levels of virus detected in supernatants and cells for up to 14 days postinfection. Treatment of GBV-B-infected hepatocyte cultures with a novel class of HCV protease inhibitor (pyrrolidine 5,5 trans-lactams) reduced viral levels by more than 2 logs. Treatment of GBV-B-infected marmosets with one such inhibitor resulted in a 3-log drop in serum viral titer over 4 days of therapy. These studies provide the first demonstration of the in vivo efficacy of a small-molecule inhibitor for HCV in an animal model and illustrate the utility of GBV-B as a surrogate animal model system for HCV.
PMCID: PMC369465  PMID: 14747571
14.  Opportunistic mothers: female marmosets (Callithrix kuhlii) reduce their investment in offspring when they have to, and when they can 
Journal of human evolution  2005;49(1):122-142.
All female primates incur energetic costs associated with producing and caring for offspring, but females belonging to the New World primate family Callitrichidae, the marmosets and tamarins, appear to face even further demands. In fact, the energetic demands of rearing callitrichid infants are thought to have led to the evolution of cooperative infant care in these species. If this explanation is true, then one might expect that natural selection should also have shaped patterns of maternal behavior to be sensitive to the costs of reproduction and equipped females to reduce their investment in offspring under certain conditions. Therefore, we examined the maternal effort and postpartum endocrine profiles of individual female marmosets (Callithrix kuhlii) across conditions that represented two hallmarks of callitrichid reproduction—conception during the early postpartum period and alloparental assistance. When females conceived during the early postpartum period and faced the upcoming demands of caring for their newly conceived litters (Study 1), they significantly reduced their caregiving effort and had significantly higher postpartum levels of estradiol relative to breeding attempts in which conception occurred later in the postpartum period. Postpartum estradiol was negatively correlated with maternal carrying effort. When experienced alloparents were present (Study 2), females again reduced their caregiving effort relative to breeding attempts in which experienced alloparents were not present. Postpartum cortisol, however, did not vary as a function of experienced alloparental assistance. The results of these studies suggest that female marmosets have been subjected to similar selection pressures as females of other primate taxa—to maximize their reproductive success by reducing their investment in offspring under the worst and best of conditions—and suggest that hormones may mediate within-female variation in maternal care. These studies also provide support for the notion that mothers are “flexible opportunists” when it comes to providing care to their young.
PMCID: PMC2987622  PMID: 15935439
Wied’s black tufted-ear marmoset; Callitrichidae; Maternal care; Postpartum conception; Lactation; Alloparental care
15.  Social and Developmental Influences on Urinary Androgen Levels in Young Male White-Faced Marmosets (Callithrix geoffroyi) 
American journal of primatology  2010;73(4):378-385.
Callitrichine primates (marmosets and tamarins) often remain in their natal groups beyond the time of sexual maturity. Although studies have characterized the development of female reproductive function in callitrichine offspring, less is known about the male reproductive development. To document reproductive development in male marmosets, we monitored urinary androgen (uA) excretion in males housed in a captive colony of white-faced marmosets (Callithrix geoffroyi). Young male marmosets showed relatively low and stable rates of uA excretion early in life, with elevated production at the end of the juvenile period (9–10 months) and again at the onset of adulthood (16 months). uA levels of adult breeding males were also measured to compare to adult-aged sons. Although breeding males did have higher uA levels than their adult-aged sons, these differences did not reach conventional levels of significance. Evidence from some other reports has suggested that androgen levels of males in other species are influenced by social factors, such as the presence of a sexually receptive female or of dependent offspring. In this study, however, uA levels did not vary, based on their mothers’ pregnancy status or the presence of younger siblings in the natal group. Patterns of androgen excretion in the white-faced marmoset roughly reflect those of other callitrichine species. Furthermore, unlike callitrichine daughters, gonadal activity in sons does not seem to be sensitive to within-group social cues.
PMCID: PMC3086337  PMID: 21328596
testosterone; male sexual development; pregnancy status; social status; younger siblings presence
16.  Prolactin's Mediative Role in Male Parenting in Parentally Experienced Marmosets (Callithrix jacchus) 
Hormones and behavior  2009;56(4):436-443.
Prolactin has been implicated in promoting paternal care behaviors but little evidence of causality has been found to date except for birds and fish. This study was designed to examine the possible causal relationships between prolactin and male parenting behaviors, reproductive hormones, and physical changes in cooperatively breeding common marmosets, Callithrix jacchus. Fifteen parentally experienced fathers were studied over three consecutive infant care periods during two weeks prior and three weeks following their mates' parturition under three treatment conditions: normal control pregnancy, decreased prolactin and elevated prolactin. The treatments significantly altered the serum prolactin levels in the fathers. Using three methods of determining a father's level of parental care: infant carrying, family effort and responsiveness to infant stimulus tests, we found that only the male response to infant stimuli was altered by the hormone treatments. Lowering prolactin significantly reduced male responsiveness to infant stimuli but elevating prolactin showed the same effect. Hormonal sampling indicated that testosterone levels showed an inverse relationship to prolactin levels during a normal peripartum period and prolactin treatment reduced this relationship. Prepartum estradiol levels were significantly elevated during the lowered prolactin treatment and estradiol was significantly lowered postpartum with the elevated prolactin treatment. Father's weight decreased significantly by the third week of infant care during the normal treatment. Males in the elevated prolactin treatment lost little or no weight from prepartum while in the lowered prolactin treatment showed the most weight loss. The present findings did not distinguish a direct causal relationship of prolactin on behavior in experienced fathers but did find an interaction with other hormones and weight gain.
PMCID: PMC2761515  PMID: 19664636
prolactin; paternal care; infant responsiveness; testosterone; estradiol; common marmoset; weight gain
17.  Novel survey method finds dramatic decline of wild cotton-top tamarin population 
Nature Communications  2010;1(3):1-7.
For conservation purposes, accurate methods are required to track cotton-top tamarins in their natural habitat. As existing census methods are not appropriate for surveying these monkeys, a lure-transect method combined with playback vocalization was used here to allow accurate counting of the animals.
The cotton-top tamarin (Saguinus oedipus) is a critically endangered primate, endemic to the tropical forests of Colombia. Population monitoring is essential to evaluate the success of conservation efforts, yet standard survey methods are ineffective because animals flee silently before they are seen. We developed a novel technique that combines the use of playbacks of territorial vocalizations with traditional transect surveys. We used remote sensing to identify potential habitat within the species' historic range, and visited the 27% that we could survey safely. Of this, only 99 km2 was extant forest, containing an estimated 2,045 animals (95% confidence interval 1,587–2,634). Assuming comparable densities in non-surveyed areas, approximately 7,394 wild cotton-top tamarins remain in Colombia. With 20–30,000 animals exported to the United States in the late 1960s, this must represent a precipitous decline. Habitat destruction and capture for the illegal pet trade are ongoing. Urgent conservation measures are required to prevent extinction in the wild.
PMCID: PMC3026645  PMID: 20975684
18.  Biphasic Malignant Testicular Sex Cord–Stromal Tumor in a Cotton-top Tamarin (Saguinus oedipus) with Review of the Literature 
Veterinary pathology  2008;45(6):922-927.
A 20-year old male cotton-top tamarin (Saguinus oedipus) was presented with unilateral enlargement of an intrascrotal testicle. Fine-needle aspiration cytology demonstrated a neoplastic population with Call-Exner-like bodies and features of malignancy. The animal was castrated, and histologic examination revealed a biphasic sex cord–stromal tumor, with one region resembling Sertoli-cell tumor and one region resembling granulosa-cell tumor, with extensive microfollicular pattern and many Call-Exner bodies. Eight months after castration, the animal was euthanized on discovery of a caudal abdominal mass that displaced organs, was highly infiltrative, and extended into the paravertebral musculature with lysis of vertebral bone. Metastases to lymph node and lung were also present. Histologic examination of the abdominal tumor showed multifocal formation of Call-Exner bodies in an otherwise highly dedifferentiated population. Positive immunolabeling for alpha inhibin confirmed the sex cord–stromal origin of the abdominal and paravertebral tumor masses. This case has similarities to malignant testicular granulosa-cell tumor of humans.
PMCID: PMC2660595  PMID: 18984797
Granulosa cell; inhibin; primates; Sertoli cell; sex cord–stromal tumor; tamarin; testis
19.  Evolutionary foundations of number: spontaneous representation of numerical magnitudes by cotton-top tamarins. 
Although animals of many species have been shown to discriminate between visual-spatial arrays or auditory-temporal sequences based on numerosity, most of the evidence for numerosity discrimination derives from experiments involving extensive laboratory training. Under these conditions, animals' discrimination of two numerosities depends on their ratio and is independent of their absolute value. It is an open question whether any untrained non-human animal spontaneously represents number in this way, as do human children and adults. We present the results of familiarization-discrimination experiments on cotton-top tamarin monkeys (Saguinus oedipus) that provide evidence for numerosity discrimination in the absence of training. Presented with auditory stimuli (speech syllables) controlled for the continuous variables of sequence duration, item duration, inter-stimulus interval and overall energy, tamarins readily discriminated sequences of 4 versus 8, 4 versus 6, and 8 versus 12 syllables. By contrast, tamarins failed to discriminate sequences of 4 versus 5 and 8 versus 10 syllables, providing evidence that their numerosity discrimination is approximate and shows the ratio signature of numerosity discrimination in humans and trained non-human animals. These results provide strong support for the hypothesis that representations of large, approximate numerosity are evolutionarily ancient and spontaneously available to non-human animals.
PMCID: PMC1691404  PMID: 12965007
20.  Novel Gamma-1 Herpesviruses Identified in Free-Ranging New World Monkeys (Golden-Handed Tamarin [Saguinus midas], Squirrel Monkey [Saimiri sciureus], and White-Faced Saki [Pithecia pithecia]) in French Guiana 
Journal of Virology  2003;77(16):9099-9105.
The recent finding of a novel Epstein-Barr virus-related lymphocryptovirus (CalHV-3) in a captive colony of common marmoset (Callithrix jacchus) in the United States modifies the view that the host range of lymphocryptovirus is restricted to humans and Old World primates. We investigated the presence of Epstein-Barr virus-related viruses in 79 samples of New World monkeys caught in the wild, including six species of the Cebidae family and one of the Callitrichidae, living in the rain forest of French Guiana. Using a degenerate consensus PCR method for the herpesvirus DNA polymerase gene, we identified three novel lymphocryptoviruses from golden-handed tamarin (Saguinus midas) of the Callitrichidae family and squirrel monkey (Saimiri sciureus) and white-faced saki (Pithecia pithecia) of the Cebidae family. With the CalHV-3 strain, these three novel viruses constitute a well-supported phylogenetic clade in the Lymphocryptovirus genus, which is clearly distinct from the lineage of Old World lymphocryptovirus, hosted by catarrhine monkeys and humans. In tamarins, the prevalence of the novel lymphocryptovirus was more than 50%, indicating that it circulates well in the wild population, perhaps due to specific ecoethological patterns such as confrontations and intergroup migration. The detection and partial molecular characterization of the polymerase gene of three novel Gamma-1-Herpesvirinae from New World monkeys caught in the wild clearly indicate that free-ranging populations of platyrrhine are natural hosts of lymphocryptoviruses. Further characterization of these novel viruses will provide new insight not only into the origin and evolution of Gammaherpesvirinae but also into their pathogenicity.
PMCID: PMC167222  PMID: 12885928
21.  The Marmoset Model of GB Virus B Infections: Adaptation to Host Phenotypic Variation▿  
Journal of Virology  2009;83(11):5806-5814.
Worldwide, approximately 170 million people are chronically infected with hepatitis C virus (HCV), and chronic infection frequently progresses to serious liver disease, including cirrhosis and hepatocellular carcinoma. GB virus B (GBV-B), the virus phylogenetically most closely related to HCV, causes hepatitis in tamarins. We have demonstrated the suitability of the tamarin as a host for GBV-B and as a surrogate nonhuman primate model for HCV infection, and we have initiated studies of GBV-B infection in a closely related species, the common marmoset (Callithrix jacchus). Here, we demonstrate that marmosets exhibit two phenotypes upon infection with GBV-B: the susceptible phenotype and the partially resistant phenotype. In addition, we identify changes that may correlate with adaptation of the virus to the partially resistant host. GBV-B was serially passaged five times through 14 marmosets as one lineage and two times through 6 marmosets as a second lineage. Virus adapted to the marmosets and eventually exhibited robust infections in two separate lineages, lineages 1 and 2. A third lineage was initiated with a molecular clone, and again, susceptible and partially resistant phenotypes were observed. Three isolates were fully sequenced (from lineage 1), and 21 nucleotide changes were observed, with six amino acid changes. We speculate that the marmoset partially resistant phenotype may be due to a polymorphism in the marmoset population that affects critical virus-host interactions and that wild-type GBV-B is capable of rapidly adapting to this altered host.
PMCID: PMC2681958  PMID: 19279089
22.  Maternal gestational androgens are associated with decreased juvenile play in white-faced marmosets (Callithrix geoffroyi) 
Hormones and behavior  2012;62(2):136-145.
Exposure to androgens during prenatal development shapes both physiological and behavioral developmental trajectories. Notably, in rhesus macaques, prenatal androgen exposure has been shown to increase rough-and-tumble play, a prominent behavioral feature in males during the juvenile period in primates. While macaques are an Old World, polygamous species with marked sexually dimorphic behavior, New World callitrichine primates (marmosets and tamarins) live in cooperative breeding groups and are considered to be socially monogamous and exhibit minimal sexual dimorphism in social play, which suggests that androgen may affect this species in different ways compared to macaques. In addition, we previously described considerable variation in maternal androgen production during gestation in marmosets. Here we tested the association between this variation and variation in offspring rough-and-tumble play patterns in both males and females. We measured testosterone and androstenedione levels in urine samples collected from pregnant marmoset mothers and then observed their offspring's play behavior as juveniles (5–10 months of age). In contrast to findings in rhesus macaques, hierarchical regression analyses showed that higher gestational testosterone levels, primarily in the second semester, were associated with decreased rough-and-tumble play in juveniles, and this relationship appears to be driven more so by males than females. We found no reliable associations between gestational androstenedione and juvenile play behavior. Our findings provide evidence to suggest that normative variation in levels of maternal androgen during gestation may influence developmental behavioral trajectories in marmosets in a way that contradicts previous findings in Old World primates.
PMCID: PMC3586234  PMID: 22705955
Rough-and-tumble play; Prenatal programming; Androstenedione; Testosterone; Intrauterine environment; Maternal androgens; Organizational effects
23.  Developmental Origins of Pregnancy Loss in the Adult Female Common Marmoset Monkey (Callithrix jacchus) 
PLoS ONE  2014;9(5):e96845.
The impact of the intrauterine environment on the developmental programming of adult female reproductive success is still poorly understood and potentially underestimated. Litter size variation in a nonhuman primate, the common marmoset monkey (Callithrix jacchus), allows us to model the effects of varying intrauterine environments (e.g. nutrient restriction, exposure to male womb-mates) on the risk of losing fetuses in adulthood. Our previous work has characterized the fetuses of triplet pregnancies as experiencing intrauterine nutritional restriction.
Methodology/Principal Findings
We used over a decade of demographic data from the Southwest National Primate Research Center common marmoset colony. We evaluated differences between twin and triplet females in the number of pregnancies they produce and the proportion of those pregnancies that ended in fetal loss. We found that triplet females produced the same number of total offspring as twin females, but lost offspring during pregnancy at a significantly higher rate than did twins (38% vs. 13%, p = 0.02). Regardless of their own birth weight or the sex ratio of the litter the experienced as fetuses, triplet females lost more fetuses than did twins. Females with a male littermate experienced a significant increase in the proportion of stillbirths.
These striking findings anchor pregnancy loss in the mother’s own fetal environment and development, underscoring a "Womb to Womb" view of the lifecourse and the intergenerational consequences of development. This has important translational implications for understanding the large proportion of human stillbirths that are unexplained. Our findings provide strong evidence that a full understanding of mammalian life history and reproductive biology requires a developmental foundation.
PMCID: PMC4037172  PMID: 24871614
24.  General Intelligence in Another Primate: Individual Differences across Cognitive Task Performance in a New World Monkey (Saguinus oedipus) 
PLoS ONE  2009;4(6):e5883.
Individual differences in human cognitive abilities show consistently positive correlations across diverse domains, providing the basis for the trait of “general intelligence” (g). At present, little is known about the evolution of g, in part because most comparative studies focus on rodents or on differences across higher-level taxa. What is needed, therefore, are experiments targeting nonhuman primates, focusing on individual differences within a single species, using a broad battery of tasks. To this end, we administered a large battery of tasks, representing a broad range of cognitive domains, to a population of captive cotton-top tamarin monkeys (Saguinus oedipus).
Methodology and Results
Using a Bayesian latent variable model, we show that the pattern of correlations among tasks is consistent with the existence of a general factor accounting for a small but significant proportion of the variance in each task (the lower bounds of 95% Bayesian credibility intervals for correlations between g and task performance all exceed 0.12).
Individual differences in cognitive abilities within at least one other primate species can be characterized by a general intelligence factor, supporting the hypothesis that important aspects of human cognitive function most likely evolved from ancient neural substrates.
PMCID: PMC2690653  PMID: 19536274
25.  Give unto others: genetically unrelated cotton-top tamarin monkeys preferentially give food to those who altruistically give food back. 
Altruistic food giving among genetically unrelated individuals is rare in nature. The few examples that exist suggest that when animals give food to unrelated others, they may do so on the basis of mutualistic or reciprocally altruistic relationships. We present the results of four experiments designed to tease apart the factors mediating food giving among genetically unrelated cotton-top tamarins (Saguinus oedipus), a cooperatively breeding New World primate. In experiment 1 we show that individuals give significantly more food to a trained conspecific who unilaterally gives food than to a conspecific who unilaterally never gives food. The apparent contingency of the tamarins' food-giving behaviour motivated the design of experiments 2-4. Results from all three experiments show that altruistic food giving is mediated by prior acts of altruistic food giving by a conspecific. Specifically, tamarins do not give food to unrelated others when the food received in the past represents the by-product of another's selfish actions (experiments 2 and 3) or when a human experimenter gives them food (experiment 4) as did the unilateral altruist in experiment 1. By contrast, if one tamarin gives another food without obtaining any immediate benefit, then the recipient is more likely to give food in return. Overall, results show that tamarins altruistically give food to genetically unrelated conspecifics, discriminate between altruistic and selfish actions, and give more food to those who give food back. Tamarins therefore have the psychological capacity for reciprocally mediated altruism.
PMCID: PMC1691522  PMID: 14667352

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