Web Box 9.1 Parental Prolactin

The hormone prolactin has hundreds of metabolic functions in mammals, as well as in birds, amphibians, and fish (Ziegler, 2000). Its most widely known function is to stimulate the mammary glands of mammalian mothers to secrete milk for dependent offspring. But, prolactin affects males as well as females through its inhibitory effects on other hormones, such as testosterone, and its effects on sexual, affiliative, and parental behavior. In an elaborate set of studies on cotton-top tamarins and common marmosets, reproductive endocrinologist Toni Ziegler and her colleagues (Ziegler et al., 1996; Ziegler and Snowdon, 2000; Snowdon and Ziegler, 2015) have investigated how patterns in levels of urinary prolactin affect both maternal and paternal caretaking and sociosexual behaviors alike.

Ziegler knew that elevated levels of prolactin and low levels of testosterone had been reported in male common marmosets which carried 10 30-day-old infants (Dixson and George, 1982). She didn’t know how prolactin levels in male caretakers in the closely related cotton-top tamarin compared to pregnant and nonpregnant females, or how variable the timing and degree of prolactin elevations were in these males. Collecting near daily urine samples from males and females housed in family groups in Charles Snowdon’s captive cotton-top colony (see Box 1.1), Ziegler first confirmed that males carrying infants had higher levels of prolactin compared to males paired with nonpregnant females, similar to what had been reported for common marmosets. The actual levels of prolactin in infant carrying fathers were similar to those of nursing females, and in both parents, prolactin levels remained high up to two weeks after infants died.

Older sons in these family groups exhibited higher prolactin levels within two weeks after the birth of their younger siblings compared to nonfathers. However, it wasn’t clear from these results whether male caretaking behavior is responsible for stimulating elevations in prolactin or whether high levels of prolactin stimulate these males to participate in infant care. To distinguish between these alternative causal scenarios, Ziegler and her colleagues examined male and female prolactin levels before their infants were born. Sure enough, compared to males paired with nonpregnant females, paternal prolactin levels turned out to be significantly higher by at least two weeks prior to the births of their offspring. Evidently, paternal prolactin levels respond to hormonal or behavioral cues from females approaching their parturition dates. Fathers are effectively hormonally “primed” to care for their infants even before they arrive.

Yet another intriguing discovery from Ziegler’s study is the finding that experienced fathers have higher prolactin levels than inexperienced fathers. Indeed, prolactin levels were positively related to paternal reproductive history, with the most reproductively experienced fathers having the highest levels of prolactin of all. This may be why reproductively inexperienced older siblings exhibit elevations in their prolactin after, but not before, new infants are born.

Exactly how reproductive experience might affect paternal prolactin levels is still not entirely clear. The fact that infant survivorship increases with both maternal and paternal reproductive experience suggests that elevations in prolactin may facilitate parental care, and therefore increase their offspring’s chances of survival.

In common marmosets, olfactory cues from the infant cause the father’s testosterone levels to lower and his estradiol and prolactin levels to rise, along with his attention to infant care (Ziegler et al., 2011). Changes in the fathers’ brains as a result of these prolactin elevations persist, even after the infant is independent and no longer requires paternal care (Woller et al., 2012).

Prolactin’s inhibitory effect on testosterone results in less sexual and aggressive behavior. If females can detect male prolactin levels through olfactory or behavioral cues, they may be more likely to entrust infants to their care. In primates like these, where male reproductive success hinges on reducing the energetic costs of reproduction to females so they can ovulate and conceive again, both male infant care and communication between mates should be under strong selection pressures. Recent findings that prolactin levels were strongly correlated among pair-bonded cotton-top tamarin males and females, and varied with the frequency of both sexual and affiliative contact (Snowdon and Ziegler, 2015) provide additional support for the interacting effects of hormones and behavior. Indeed, understanding the hormonal mechanisms underlying male parental behavior is a necessary step in testing evolutionary hypotheses about behavioral adaptations.

Ziegler’s long-standing quest to decipher how hormones and behavior interact is not limited to prolactin and parenting. Nor is it limited to cotton-top tamarins in captivity. She is one of a handful of reproductive endocrinologists whose pioneering efforts have led to the development of noninvasive techniques for getting hormonal information from wild and captive primates alike. Prolactin, like many other hormones, gets metabolized into unrecognizable forms in primate feces, and can therefore only be measured in blood or urine. However, a few of the key hormones produced by the gonads (testes and ovaries), such as testosterone, estrogen, and progesterone, and by the adrenal glands, such as cortisol, can also be measured in feces. Thanks to scientists like Ziegler, these gonadal and adrenal hormones are now being monitored in a wide range of wild primates (Chapter 12). Results from these studies provide crucial information on the interactions between the proximate and ultimate mechanisms involved in regulating behavior.

Bibliography to Web Box 9.1

Dixson, A. F. and George, L. (1982). Prolactin and parental behaviour in a male New World primate. Nature 299: 551–553.

Snowdon, C. T. and Ziegler, T. E. (2015). Variation in prolactin is related to variation in sexual behavior and contact affiliation. PLoS ONE 10: e0120650.

Woller, M. J., Sosa, M. E., Chiang, Y., Prudom, S. L., Keelty, P., Moore, J. E., et al. (2012). Differential hypothalamic secretion of neurocrines in male common marmosets: Parental experience effects? Journal of Neuroendocrinology 24: 413–421.

Ziegler, T. E. (2000). Hormones associated with non-maternal infant care: A review of mammalian and avian studies. Folia Primatologica 71: 6–21.

Ziegler, T. E. and Snowdon, C. T. (2000). Preparental hormone levels and parenting experience in male cotton-top tamarins, Saguinus oedipus. Hormones and Behavior 38: 159–167.

Ziegler, T. E., Wegner, F. H., and Snowdon, C. T. (1996). Hormonal responses to parental and nonparental conditions in male cotton-top tamarins, Saguinus oedipus, a New World primate. Hormones and Behavior 30: 287–297.

Ziegler, T. E., Peterson, L. J., Sosa, M. E., and Barnard, A. M. (2011). Differential endocrine responses to infant odors in common marmoset (Callithrix jacchus) fathers. Hormones and Behavior 59: 265–270.