Maternal gestational androgens are associated with decreased juvenile play in white-faced marmosets (Callithrix geoffroyi)

Abstract

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.

Fig. 1

Urinary concentrations of A⁴ (panel a) and T-DHT (panel b) for each pregnancy relative to birth, grouped by female. Hormones were averaged in 10-day blocks. The first point represents estimated date of conception. Day “0” represents date of birth. Dashed vertical lines represent semester divisions.

Fig. 2

Rates of overall play, play receptions, and play initiations with all members of the family group as a function of first semester gestational T-DHT (a-c) and second semester T-DHT (d-f). Play behaviors (on vertical axes) are average frequencies per 20-min focal observation period. Open circles represent males; closed circles represent females. *Indicates instance in which an outlier was removed.

Fig. 3

Play behaviors with all siblings and male siblings as a function of T-DHT during the first (a-c) and second (d-f) semesters of gestation. Play behaviors (on vertical axes) are average frequencies per 20-min focal observation period. Open circles represent males; closed circles represent females. *Indicates instance in which an outlier was removed.