Number of ovulations in the marmoset monkey (Callithrix jacchus): Relation to body weight, age and repeatability

Tardif, Suzette D.; Jaquish, Cashell E.

doi:10.1002/(sici)1098-2345(1997)42:4<323::aid-ajp7>3.0.co;2-z

Cited by 55 publications

(47 citation statements)

References 19 publications

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“…Our results are also consistent with evidence that physiological components of callitrichid maternal investment vary with maternal condition. In common marmosets, for example, there was more within-than betweenfemale variation in the number of ova females ovulated per cycle, and individual females ovulated significantly fewer ova at lower body weights than they did at higher body weights (Tardif and Jaquish, 1997). Similarly, Bales et al (2001) reported that female golden lion tamarins at lower body weights gave birth to smaller litters than females at higher body weights.…”

Section: Discussionmentioning

confidence: 99%

Opportunistic mothers: female marmosets (Callithrix kuhlii) reduce their investment in offspring when they have to, and when they can

Fite

Patera

French

et al. 2005

Journal of Human Evolution

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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.

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Section: Discussionmentioning

confidence: 99%

Opportunistic mothers: female marmosets (Callithrix kuhlii) reduce their investment in offspring when they have to, and when they can

Fite

Patera

French

et al. 2005

Journal of Human Evolution

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“…Older marmosets with fewer nonovulatory antral follicles also have a tendency to have fewer preovulatory follicles, implying a lower ovulation rate. This finding contradicts that of Tardif et al [28], who reported no relationship between ovulation rate and age in marmosets, although this discrepancy may be a consequence of differences in sampling techniques and the low number of subjects in that analysis (n ϭ 11). The decrease in numbers of preovulatory follicles in older marmosets observed in the present study implies that these animals will have smaller litters in the second half of their reproductive life, before reaching senescence.…”

Section: Discussionmentioning

confidence: 67%

“…Captive marmosets are however capable of producing viable offspring up to at least 11 yr of age (personal observations). Tardif et al [28] reported that the greatest source of variability of ovulation rate in marmosets is within females (i.e., between successive cycles) rather than between females. The variation in ovulation rate in individual marmosets is positively correlated with body weight, suggesting that reproductive output is related to energy availability [28].…”

Section: Discussionmentioning

confidence: 99%

Changes in Follicle-Stimulating Hormone and Follicle Populations During the Ovarian Cycle of the Common Marmoset1

Gilchrist¹,

Wicherek²,

Heistermann³

et al. 2001

Biology of Reproduction

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The common marmoset (Callithrix jacchus) belongs to the family Callitrichidae, the only anthropoid primates with a high and variable number of ovulations (one to four). An understanding of folliculogenesis in this species may provide some insight into factors regulating multiple follicular growth in primates. The aims of this study were to characterize in detail changes in the antral follicle population at different stages of the ovarian cycle, to characterize the marmoset FSH profile, and to relate cyclic changes in FSH to changes in follicle sizes and circulating estradiol concentrations. Fifty-five pairs of ovaries were collected (32 of which were at five distinct stages of the cycle) from adult marmosets, and antral follicles were manually excised and separated into four size groups. Daily urinary FSH and plasma estradiol and progesterone concentrations from Day 0 of the follicular phase to 2 days postovulation were measured in 22 marmosets using enzyme immunoassays. The FSH profile revealed two distinct peaks, on Days 2 and 6, during the 10-day follicular phase, with a marginal periovulatory increase on Days 9 and 10. Estradiol levels rose significantly (P:< 0.05) above baseline (Days 1-4) on Day 5 and continuously increased to a peak on the day preceding ovulation (Days 8 and 9). Follicle dissection revealed a high (mean = 68) and variable (range, 14-158) total number of antral follicles >0.6 mm. The number of antral follicles significantly declined (P: < 0.001) with age. The number of preovulatory follicles (>2 mm) was positively correlated with the number of antral follicles (P: < 0. 001) and tended to be negatively related to age (P: = 0.06). The number of antral follicles did not vary significantly with stage of the ovarian cycle, although the follicle size distribution was cycle-stage dependent (P: < 0.05). Follicles >1.0 mm appeared only in the follicular phase, and preovulatory follicles (>2.0 mm) appeared only at the end of the follicular phase (Days 7-9). The Day 2 FSH peak corresponded to emergence of a population of medium-size antral follicles, and the Day 6 peak was consistent with rising estradiol levels and appearance of the preovulatory follicles. These results suggest that some aspects of marmoset folliculogenesis are comparable to those in Old World primates, including the absence of multiple follicular waves and the appearance of an identifiable dominant follicle in the midfollicular phase. However, the midphase FSH peak, multiple dominant follicles, and abundance of nonovulatory antral follicles differ strongly from the pattern in Old World primates and humans. The findings are discussed in relation to the regulation of growth of multiple ovulatory follicles and provide the basis for further studies on factors influencing the dynamics of follicular growth and development in this species.

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“…This would reinforce the selective advantage of twinning over singleton births, as well as loss of lactational anovulation. In captive marmoset populations there is a significant positive correlation between the number of ovulations (one or two versus three or four) and increased maternal weight when examined by logistic regression (8). Because obligate twinning and shortened interbirth intervals would increase anabolic metabolic demands on breeding females, we, like others have in the past (76,77), view the preadaptation for paternal care concomitant with alloparenting by siblings and reproductive suppression of subordinates as highly effective.…”

Section: Discussionmentioning

confidence: 97%

“…Although other anthropoid primates occasionally produce twins and rarely higher-order litters, callitrichines are the only anthropoid primates having an "obligate multiples phenotype" resulting from ovulation of multiple ova per cycle (8,9). Dichorionic, dizygotic (DZ) twins comprise the predominant litter size in the wild, although triplets have been reported (10), and twin, triplet, and quadruplet litters are frequently reported in captive colonies.…”

mentioning

confidence: 99%

Evolutionary genetics and implications of small size and twinning in callitrichine primates

Harris

Tardif

Vinař

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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New World monkeys (NWMs) are characterized by an extensive size range, with clawed NWMs (subfamily Callitrichinae, or callitrichines) such as the common marmoset manifesting diminutive size and unique reproductive adaptations. Perhaps the most notable of these adaptations is their propensity toward multiple gestations (i.e., dichorionic twins and trichorionic triplets). Indeed, with the exception of Goeldi's monkey (Callimico), callitrichine singleton pregnancies rarely occur. Multiple gestations seem to have coevolved with a suite of reproductive adaptations, including hematopoetic chimerism of siblings, suppression of reproduction in nondominant females, and cooperative alloparenting. The sequencing of the common marmoset (Callithrix jacchus) genome offers the opportunity to explore the genetic basis of these unusual traits within this primate lineage. In this study, we hypothesized that genetic changes arising during callitrichine evolution resulted in multiple ovulated ova with each cycle, and that these changes triggered adaptations that minimized complications common to multiple gestations in other primates, including humans. Callitrichine-specific nonsynonymous substitutions were identified in GDF9, BMP15, BMP4, and WFIKKN1. WFIKKN1, a multidomain protease inhibitor that binds growth factors and bone morphogenetic proteins, has nonsynonymous changes found exclusively in common marmosets and other tested callitrichine species that twin. In the one callitrichine species that does not produce twins (Callimico), this change has reverted back to the ancestral (nontwinning) primate sequence. Polymorphisms in GDF9 occur among human cohorts with a propensity for dizygotic twins, and polymorphisms in GDF9 and BMP15 are associated with twinning in sheep. We postulate that positive selection affected NWM growth patterns, with callitrichine miniaturization coevolving with a series of reproductive adaptations.reproductive biology | primate evolution

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Number of ovulations in the marmoset monkey (Callithrix jacchus): Relation to body weight, age and repeatability

Cited by 55 publications

References 19 publications

Opportunistic mothers: female marmosets (Callithrix kuhlii) reduce their investment in offspring when they have to, and when they can

Opportunistic mothers: female marmosets (Callithrix kuhlii) reduce their investment in offspring when they have to, and when they can

Changes in Follicle-Stimulating Hormone and Follicle Populations During the Ovarian Cycle of the Common Marmoset1

Evolutionary genetics and implications of small size and twinning in callitrichine primates

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