Social effects via olfactory sensory stimuli on reproductive function and dysfunction in cooperative breeding marmosets and tamarins

Abstract

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.

Figure 1

A female common marmoset rubs scent secretions from the anogenital/suprapubic scent glands, mixed with urine, on a reagent stopper top. Once deposited these scent secretions can be diluted and transferred for storage and presentation to a recipient.

Figure 2

Histological presentation of the nasal system in the common marmoset. Arrow points to the vomeronasal organ (VNO) embedded between the sinuses. The marmoset VNO has all the specific structures to suggest functionality.

Figure 3

Behavioral responses in male common marmosets to isolated periovulatory scents from a novel female versus a vehicle control scent. Frequence or latency was plotted against the scent condition received. Data from Ziegler et al., 2005, Hormones and Behavior 47, 56–64.

Figure 4

Significant differences in testosterone but not cortisol levels in male common marmosets following isolated scent exposure to a novel periovulatory scent relative to the vehicle control. Males showed significant differences in testosterone by social condition. Data from Ziegler et al., 2005, Hormones and Behavior 47, 56–64.

Figure 5

Inhibition of ovulation occurs in female cotton-top tamarin daughters well after puberty. Levels of urinary luteinizing hormone (LH) and estrogens (E1G) while the daughter lived with the family and when she was paired with a male (date 7–22). An LH peak can be seen on day 8–3 and chorionic gonadotropin levels were elevated by day 8–27 indicating pregnancy.

Figure 6

Time to ovulation from pairing with a male in female cotton-top tamarins. Exposed daughters were exposed twice daily to wooden dowls containing their mother’s scents while control females had no scent transfer. No female who received mother’s scent ovulated during that time. Time to ovulation was significantly longer for the females received their mother’s scent. Data presented in Savage et al., 1988, American J Primatol. 14, 345–359.

Figure 7

Cotton-top tamarin males show increased androgen excretion (testosterone and DHT) in the five days pre- and post-ovulation in their mate during the postpartum period. Zero indicates the day of ovulation in the mate (x-axis). Males were caring for infants during this time. Data from Ziegler et al., 2004 Amer J Primatol 64, 57–69.

Figure 8

Common marmoset fathers show decreased circulating androgen and increased estrogen production 30 minutes following smelling their own infant scent compared to a novel infant’s scent of the same age. The scent was collected from infants 5–10 days of age and presented to the males in an isolated room. The x-axis indicates the vehicle, own, or novel treatment the males received during the scent presentation. Data from Ziegler et al. 2011, Hormones and Behavior 59, 265–270.