Publications

The formation of viable genetic chimeras in mammals through the transfer of cells between siblings in utero is rare. Using microsatellite DNA markers, we show here that chimerism in marmoset (Callithrix kuhlii) twins is not limited to blood-derived hematopoietic tissues as was previously described. All somatic tissue types sampled were found to be chimeric. Notably, chimerism was demonstrated to be present in germ-line tissues, an event never before documented as naturally occurring in a primate. In fact, we found that chimeric marmosets often transmit sibling alleles acquired in utero to their own offspring. Thus, an individual that contributes gametes to an offspring is not necessarily the genetic parent of that offspring. The presence of somatic and germ-line chimerism may have influenced the evolution of the extensive paternal and alloparental care system of this taxon. Although the exact mechanisms of sociobiological change associated with chimerism have not been fully explored, we show here that chimerism alters relatedness between twins and may alter the perceived relatedness between family members, thus influencing the allocation of parental care. Consistent with this prediction, we found a significant correlation between paternal care effort and the presence of epithelial chimerism, with males carrying chimeric infants more often than nonchimeric infants. Therefore, we propose that the presence of placental chorionic fusion and the exchange of cell lines between embryos may represent a unique adaptation affecting the evolution of cooperative care in this group of primates.

Although reports on colony demographics for a variety of callitrichid species are available in the literature, to date there has not been a detailed examination of Wied's black tufted-ear marmoset (Callithrix kuhlii). The purpose of this study is to present colony demographics for C. kuhlii from the University of Nebraska at Omaha's Callitrichid Research Center from 1991 to 2002. C. kuhlii are currently held in a number of zoological parks in the United States and abroad; however, the University of Nebraska at Omaha held the only breeding colony in North America. Here we report data on lifespan, sex ratio, litter size, and interbirth interval (IBI) for that captive breeding colony.

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.

The proximate mechanisms that regulate transitions in mammalian female reproductive effort have not been widely studied. However, variation in circulating levels of the androgenic steroid hormone testosterone (T) appears to mediate a trade-off between investment in current and future offspring in males [Ketterson, E.D., Nolan, V., Jr., 1992. Hormones and life histories: an integrative approach. Am. Nat. 140, S33-S62; Ketterson, E.D., Nolan, V., Jr., 1994. Hormones and life histories: an integrative approach. In: L.A. Real (Ed.), Behavioral Mechanisms in Evolutionary Ecology, University of Chicago Press, Chicago, pp. 327-353; Ketterson, E. D., Nolan, V., Jr., 1999. Adaptation, exaptation, and constraint: A hormonal perspective. Am. Nat. 154S, S4-S25]. The purpose of this study was to investigate the possibility that T is also associated with transitions in the reproductive effort of females, by examining the relationship between urinary T excretion, maternal caregiving behavior, and the timing of the postpartum conception in female Wied's black tufted-ear marmosets (Callithrix kuhlii). We examined the maternal carrying effort and peripartum T profiles of six females across two conditions: (1) when they conceived during the period of infant dependence (DPID), such that gestation was coupled with lactation; and (2) when the same females conceived after the period of infant dependence (APID). We also assessed the relationship between postpartum T levels and caregiving effort. When female marmosets conceived DPID, they dramatically reduced their caregiving effort, and had higher levels of urinary T, relative to when they conceived APID. Further, the litter-to-litter changes in maternal caregiving effort that we observed were related to variation in urinary T excretion; as weekly levels of urinary T excretion increased, concurrent caregiving effort declined. Our results suggest that variation in T secretion may regulate transitions in female reproductive behavior, and that the regulation of male and female parental behavior may be mediated by homologous neuroendocrine mechanisms.

Androgen is associated with the expression of male-typical behavior, including aggressive behavior, but high levels of androgen may be incompatible with other behavioral systems, such as paternal care. In a variety of species of birds that display paternal care, testosterone (T) levels in males are maintained at low levels, and these levels rise only in response to direct agonistic challenges. This idea has not been thoroughly studied in mammals with biparental care, and we exposed male marmosets (Callithrix kuhlii), a monogamous and biparental primate to aggressive interactions with unfamiliar intruders. Urinary levels of T and cortisol (CORT) were monitored prior to and following these interactions. Baseline T was not correlated with variation in aggression in either residents or intruders, and CORT was not affected by the encounters. However, males responded to an encounter with male intruders with changes in T that correlated with the level of aggression displayed by the resident male during the trial. Encounters with male intruders that elicited high frequencies of aggressive displays by the male resident were associated with increased T 2-6 h and 24 h following the encounter, and encounters that had few aggressive displays resulted in no change or a decrease in T concentrations. Intruders did not demonstrate a significant relationship between T and aggression. Thus, the magnitude of the hormonal response is dependent on the intensity of aggression during a male-male encounter, suggesting that elevated androgens are likely to be a consequence, rather than a cause, of aggressive interactions in marmosets.