Independent and additive contributions of postvictory testosterone and social experience to the development of the winner effect

Abstract

The processes through which salient social experiences influence future behavior are not well understood. Winning fights, for example, can increase the odds of future victory, yet little is known about the internal mechanisms that underlie such winner effects. Here, we use the territorial California mouse (Peromyscus californicus) to investigate how the effects of postvictory testosterone (T) release and winning experience individually mediate positive changes in future winning ability and antagonistic behavior. Male mice were castrated and implanted with T capsules to maintain basal levels of this hormone. We found that males form a robust winner effect if they win three separate territorial disputes and experience a single T surge roughly 45 min after each encounter. Meanwhile, males exhibit only an intermediate winner effect if they either 1) acquire three previous wins but do not experience a change in postvictory T or 2) acquire no previous wins but experience three separate T pulses. The results indicate that the effect of postvictory T must be coupled with that of winning experience to trigger the maximum positive shift in winning ability, which highlights the importance of social context in the development of the winner effect. At the same time, however, postvictory T and winning experience are each capable of increasing future winning ability independently, and this finding suggests that these two factors drive plasticity in antagonistic behavior via distinct mechanistic channels. More broadly, our data offer insight into the possible ways in which various species might be able to adjust their behavioral repertoire in response to social interactions through mechanisms that are unlinked from the effects of gonadal steroid action. Copyright © 2011 by The Endocrine Society.