Pre-natal Hormones Shape Female Social Interactions

In many mammals the female uterus is divided into two horns, a right and a left. Several embryos develop along the length of each horn. For example, a pregnant dog might have four fetuses developing in the right uterine horn and three more developing in the left horn. Thus, each fetus has neighbors. However, the in utero environment is not homogeneous. A female fetus surrounded by two male siblings will be exposed to increased testosterone levels (androgens) produced by her brothers to be. Such females are masculinized to varying degrees.

In rodents, one of the traits associated with female masculinization is a greater anogenital distance (the distance between the anal opening and the vaginal opening). Masculinized female offspring also exhibit more play-fighting, which is associated with aggressiveness. Non-masculinized females typically engage in more “sociopositive” behaviors. Are there any lasting effects of female masculinization in adults, and do those effects alter fitness?

Daniel Blumstein and his colleagues from the University of California (LA) set out to answer these questions in a population of yellow-bellied marmots (Marmota flaviventris) in Colorado (Figure 1). This population has been studied extensively since 2002 and all the marmots in 10 social groups are individually marked. Juveniles were live trapped as soon as the emerged from the natal den, marked, and their anogenital distance recorded. The social behaviors of 202 female colony members were monitored from April to September for seven years.

MiguelVieira
Figure 1. A yellow-bellied marmot (Marmota flaviventris) on a talus slope in the Sierra Nevada Mountains (From Flickr/Miguel Vieira)

Females with larger anogenital distances were assumed to have been masculinized
in utero. Interestingly, masculinized females initiated more play and played with more unique partners (Figure 2). They also initiated more allogrooming (grooming another individual). Males typically engage in more allogrooming and playfighting and both behaviors are controlled by androgens (In previous studies, females who were given excess testosterone also engaged in more male-like behaviors).

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Figure 2. The relationship between anogenital distance and play (left) and sociopositive behaviors (right). (From Monclus et al., 2011)

Playfighting in young marmots is similar to the agonistic behaviors of adults. Thus, it is possible that young masculinized females that engage in these behaviors may gain a competitive advantage over other females later in life. However, masculinized yearling females did not exhibit higher levels of male-like behaviors.

Finally, masculinized females interacted with more individuals and showed more willingness to explore their environment; exploration is a typically male behavior in marmots. This may explain why previous studies showed that masculinized females dispersed at higher rates that non-masculinized females. Thus, the
in utero environment can have lasting effects on female behavior.

References
Monclus, R., Cook, T., & Blumstein, D. (2011). Masculinized female yellow-bellied marmots initiate more social interactions Biology Letters DOI: 10.1098/rsbl.2011.0754