Pair bonding prevents reinforcing effects of testosterone in male California mice in an unfamiliar environment

Abstract

Testosterone (T) can be released by stimuli such as social interactions, and thereby influence future social behaviours. Because the reinforcing effects of T can induce preferences for specific environmental locations, T has the potential to alter behaviour through space use. In a monogamous species, this T pulse may contribute differently to space use in sexually naive (SN) and pair-bonded (PB) males: SN males may be more likely to explore new areas to set up a territory than PB males, which are more likely to defend an existing, established territory. In this study, we test for variation in T-driven space use by examining variation in the formation of conditioned place preferences (CPPs) in SN and PB male California mice. In the threechambered CPP apparatus, subcutaneous administrations of physiological levels of T were used to repeatedly condition SN and PB males to a side chamber, which is an unfamiliar/neutral environment. The final tests revealed that T-induced CPPs in the side chamber are developed in SN, but not PB males. This study fills a gap in our knowledge about plasticity in the rewarding nature of T pulses, based on past social experience.

Testosterone pulses at the nest site modify ultrasonic vocalization types in a monogamous and territorial mouse

“…Moreover, it mimics natural changes in T found in intact California mice after winning a male–male encounter (Fuxjager et al, ; Marler et al, ; Oyegbile & Marler, ) and in male–female encounters (X Zhao & CA Marler, unpublished). On a behavioral level, this dose increases future ability to win in male–male encounters (i.e., Fuxjager, Montgomery, et al, ; Fuxjager, Oyegbile, et al, ; Trainor et al, ), induces conditioned place preferences (Zhao & Marler, ), and alters USVs in the laboratory (Pultorak et al, ).…”

“…Transient increases in T likely occur in California mice in natural settings in the field, as elegantly described by Wingfield and others for avian species (Wingfield et al, ). Strong evidence, however, in the monogamous and territorial California mouse ( Peromyscus californicus ) supports the robust behavioral effects of one to three transient increases in T via injections with effects ranging from rapid effects (20 min) (Pultorak, Fuxjager, Kalcounis‐Rueppell, & Marler, ) to more long term, and even cumulative effects, up to at least a week (Fuxjager, Oyegbile, & Marler, ; Pultorak et al, ; Trainor, Bird, & Marler, ; Zhao & Marler, ). After a male–male encounter, a transient increase in T is released in males that helps to drive development of the winner effect (increased ability to win based on previous wins) (Fuxjager, Montgomery, & Marler, ; Fuxjager, Oyegbile, et al, ; Oyegbile & Marler, ; Trainor et al, ).…”

“…A single transient increase in T of the same magnitude can rapidly inhibit USVs in pair‐bonded (but not unpaired) male California mice when exposed to an unfamiliar female of reproductive age (Pultorak et al, ). Moreover, three transient increases in T over a week can result in the development of a preference for a specific location (conditioned place preference; Zhao & Marler, ) in addition to the previously mentioned winner effect. However, the effects of T in the form of either pulses or long‐term implants in this monogamous species have not been studied in the field, or in the context of the pair bond itself, and its associated social complexities.…”

“…In the current study, we examined the enduring effects of three injections of either T or saline over seven days, with a minimum of one day between injections, on USV production (as part of a larger ongoing field study) in California mice. All injections were conducted at the nest site of the male–female dyad, thus potentially conditioning them to the nest site (Zhao & Marler, ). We used a similar pattern of T administration that mimics natural changes as previously used in the laboratory to examine other changes in behavior (e.g., Fuxjager, Oyegbile, et al, ; Fuxjager, Montgomery, et al, ; Trainor & Marler, ; Trainor et al, ; Gleason et al, ; Zhao & Marler, ).…”

“…All injections were conducted at the nest site of the male–female dyad, thus potentially conditioning them to the nest site (Zhao & Marler, ). We used a similar pattern of T administration that mimics natural changes as previously used in the laboratory to examine other changes in behavior (e.g., Fuxjager, Oyegbile, et al, ; Fuxjager, Montgomery, et al, ; Trainor & Marler, ; Trainor et al, ; Gleason et al, ; Zhao & Marler, ). We combined this with previously used techniques for studying USVs under field conditions in which both sexes have been discovered to produce USVs that can be recorded remotely and used as a measure of mouse social behavior (Briggs & Kalcounis‐Rueppell, ).…”