Conditioned preferences: Gated by experience, context, and endocrine systems.

Central to the navigation of an ever-changing environment is the ability to form positive associations with places and conspecifics. The functions of location and social conditioned preferences are often studied independently, limiting our understanding of their interplay. Furthermore, a de-emphasis on natural functions of conditioned preferences has led to neurobiological interpretations separated from ecological context. By adopting a naturalistic and ethological perspective, we uncover complexities underlying the expression of conditioned preferences. Development of conditioned preferences is a combination of motivation, reward, associative learning, and context, including for social and spatial environments. Both social- and location-dependent reward-responsive behaviors and their conditioning rely on internal state-gating mechanisms that include neuroendocrine and hormone systems such as opioids, dopamine, testosterone, estradiol, and oxytocin. Such reinforced behavior emerges from mechanisms integrating past experience and current social and environmental conditions. Moreover, social context, environmental stimuli, and internal state gate and modulate motivation and learning via associative reward, shaping the conditioning process. We highlight research incorporating these concepts, focusing on the integration of social neuroendocrine mechanisms and behavioral conditioning. We explore three paradigms: 1) conditioned place preference, 2) conditioned social preference, and 3) social conditioned place preference. We highlight nonclassical species to emphasize the naturalistic applications of these conditioned preferences. To fully appreciate the complex integration of spatial and social information, future research must identify neural networks where endocrine systems exert influence on such behaviors. Such research promises to provide valuable insights into conditioned preferences within a broader naturalistic context.

Chronic intranasal oxytocin increases acoustic eavesdropping and adult neurogenesis.

Social information gathering is a complex process influenced by neuroendocrine-modulated neural plasticity. Oxytocin (OXT) is a key regulator of social decision-making processes such as information gathering, as it contextually modulates social salience and can induce long-term structural plasticity, including neurogenesis. Understanding the link between OXT-induced plasticity and communicative awareness is crucial, particularly because OXT is being considered for treatment of social pathologies. We investigated the role of chronic OXT-dependent plasticity in attention to novel social information by manipulating the duration of time following cessation of intranasal treatment to allow for the functional integration of adult-born neurons resulting from OXT treatment. Following a 3-week delay, chronic intranasal OXT (IN-OXT) increased approach behavior of both female and male mice towards aggressive vocal playbacks of two unseen novel conspecifics, while no effect was observed after a 3-day delay. Immature neurons increased in the ventral hippocampus of females and males treated with chronic IN-OXT after the 3-week delay, indicating a potential association between ventral hippocampal neurogenesis and approach/acoustic eavesdropping. The less the mouse approached, the higher the level of neurogenesis. Contrary to expectations, the correlation between ventral hippocampal neurogenesis and approach behavior was not affected by IN-OXT, suggesting that other plasticity mechanisms underlie the long-term effects of chronic OXT on social approach. Furthermore, we found a negative correlation between ventral hippocampal neurogenesis and freezing behavior. Overall, our results demonstrate that chronic IN-OXT-induced long-term plasticity can influence approach to vocal information and we further reinforced the link between neurogenesis and anxiety.

Acute intranasal oxytocin dose enhances social preference for parents over peers in male but not female peri-adolescent California mice (Peromyscus californicus).

Peri-adolescence is a critical developmental stage marked by profound changes in the valence of social interactions with parents and peers. We hypothesized that the oxytocin (OXT) and vasopressin (AVP) systems, known for influencing social behavior, would be involved in the maintenance and breaking of bonding behavior expressed by very early peri-adolescent males and females. In rodents, OXT is associated with mother-pup bonding and may promote social attachment to members of the natal territory. AVP, on the other hand, can act in contrasting ways to OXT and has been associated with aggression and territoriality. Specifically, we predicted that in peri-adolescent male and female juveniles of the biparental and territorial California mouse (Peromyscus californicus), a) OXT would increase the social preferences for the parents over unfamiliar age-matched peers (one male and one female), and b) AVP would break the parent-offspring bond and either increase time in the neutral chamber and/or approach to their unfamiliar and novel peers. We examined anxiety and exploratory behavior using an elevated plus maze and a novel object task as a control. Peri-adolescent mice were administered an acute intranasal (IN) treatment of 0.5 IU/kg IN AVP, 0.5 IU/kg IN OXT, or saline control; five minutes later, the behavioral tests were conducted. As predicted, we found that IN OXT enhanced social preference for parents; however, this was only in male and not female peri-adolescent mice. IN AVP did not influence social preference in either sex. These effects appear specific to social behavior and not anxiety, as neither IN OXT nor AVP influenced behavior during the elevated plus maze or novel object tasks. To our knowledge, this is the first evidence indicating that OXT may play a role in promoting peri-adolescent social preferences for parents and delaying weaning in males.

Transmission of paternal retrieval behavior from fathers to sons in a biparental rodent.

Transmission of maternal behavior across generations occurs, but less is known about paternal behavior. In biparental species like the California mouse (Peromyscus californicus), paternal care contributes to the well-being of offspring with lasting consequences on the brain and behavior. Paternal huddling/grooming behavior can be passed on to future generations, but whether paternal retrieval, which removes young from potential harm, is transmitted independently is unclear. We manipulated paternal retrieval experience through pup displacement manipulations, then examined whether males exposed to higher levels of paternal retrieval in development altered their adult retrieval behavior with their offspring. Males exposed to heightened paternal retrievals, as compared to reduced retrievals, retrieved their offspring more often but huddled/groomed offspring less during undisturbed natural observations. No differences were observed following a pup displacement challenge. The high paternal retrieval group also exhibited more physical activity and stereotypy. Our results are consistent with the hypothesis that paternal retrieval levels are transmitted across generations and may function via mechanisms separate from huddling/grooming. One modifying factor may be anxiety because increased activity and stereotypy occurred in the high retrieval group. We speculate how the transmission of paternal retrievals may inform a protective parenting style.

The challenge hypothesis revisited: Focus on reproductive experience and neural mechanisms.

Our review focuses on findings from mammals as part of a Special Issue "30th Anniversary of the Challenge Hypothesis". Here we put forth an integration of the mechanisms through which testosterone controls territorial behavior and consider how reproductive experience may alter these mechanisms. The emphasis is placed on the function of socially induced increases in testosterone (T) pulses, which occur in response to social interactions, as elegantly developed by Wingfield and colleagues. We focus on findings from the monogamous California mouse, as data from this species shows that reproductive status is a key factor influencing social interactions, site fidelity, and vigilance for offspring defense. Specifically, we examine differences in T pulses in sexually naïve versus sexually experienced pair bonded males. Testosterone pulses influence processes such as social decision making, the winner-challenge effect, and location preferences through rewarding effects of T. We also consider how social and predatory vigilance contribute to T pulses and how these interactions contribute to a territory centered around maximizing reproduction. Possible underlying mechanisms for these effects include the nucleus accumbens (rewarding effects of testosterone), hippocampus (spatial memories for territories), and the bed nucleus of the stria terminalis (social vigilance). The development of the challenge effect has provided an ideal framework for understanding the complex network of behavioral, environmental, physiological and neural mechanisms that ultimately relates to competition and territoriality across taxa. The opportunity to merge research on the challenge effect using both laboratory and field research to understand social behavior is unparalleled.

Testosterone-related behavioral and neural mechanisms associated with location preferences: A model for territorial establishment.

Territoriality is an adaptive behavioral trait that is important for animal's fitness and there still remains much to learn about the proximate mechanisms underlying the development of territoriality. We speculate that the formation of a conditioned place preference (CPP), an increased time allocation to the environment where a rewarding experience occurred, contributes to territoriality. Testosterone (T) plays an important role in modulating territorial behaviors and T pulses can induce a CPP. We confirmed previous findings in California mice (Peromyscus californicus) that T pulses can induce a CPP in singly-housed, but not group-housed males. Housing singly may be similar enough to dispersal in nature to initiate similar hormonal and neuroanatomical changes needed for the development of territoriality. We further revealed that T pulses interact with the single housing experience and appear to enhance the motivation to be aggressive towards a stimulus male. On a neural level, being singly housed upregulated levels of androgen receptors in the preoptic area, which positively correlated with the strength of the CPP. We speculate that this change in androgen sensitivity in the preoptic area is characteristic of males that have dispersed, making them more sensitive to T pulses. Also, single housing increased markers of synaptic plasticity in the nucleus accumbens, ventral and dorsal hippocampus, neural changes that may be associated with dispersal, reproduction and territory establishment. These behavioral and neural changes may reflect the life history transition from residing in the natal territory to dispersing and establishing a new territory.

Rapid effects of testosterone on social decision-making in a monogamous California mice (Peromyscus californicus).

Social animals must cope with challenges and opportunities by adjusting how they react to a salient stimulus. Here we use California mice (Peromyscus californicus) and investigate the mechanisms underlying social decision-making by studying (i) rapid effects of testosterone (T) pulses on a male's decisions to approach a novel male (challenge) versus a receptive female (opportunity), and (ii) whether social experience shapes how such effects are manifested. In Experiment 1, we found that sexually naïve males administered saline injections preferentially approached unfamiliar females over unfamiliar males, in contrast, 10 min after receiving a single T-injection, males expressed a preference for approaching unfamiliar males. Such an effect of T only occurred in sexually naïve males, but not pair-bonded males, suggesting that the rapid effects of T on approach behavior may rely on the pair-bonding experiences. Experiment 2 investigated social decision-making across three repeated exposures to the challenge/opportunity situations. Only the initial decision, approach to the challenge, predicted future aggressive behaviors, and such an effect relied on the rapid actions of T. We also found that experience with the controlled challenge situation (the male intruder was restrained behind a wire mesh) dampened the approach to the male side (potential threat) when later exposed to the same conditions. This suggests that a resident's motivation to defend against a threatening individual may decrease as the threat posed by the "neighbors" is reduced. Overall rapid effects of post-encounter T pulses may play important roles in influencing behavioral decisions during social interactions.

What can animal research tell us about the link between androgens and social competition in humans?

A contribution to a special issue on Hormones and Human Competition. The relationship between androgenic hormones, like testosterone (T), and aggression is extensively studied in human populations. Yet, while this work has illuminated a variety of principals regarding the behavioral and phenotypic effects of T, it is also hindered by inherent limitations of performing research on people. In these instances, animal research can be used to gain further insight into the complex mechanisms by which T influences aggression. Here, we explore recent studies on T and aggression in numerous vertebrate species, although we focus primarily on males and on a New World rodent called the California mouse (Peromyscus californicus). This species is highly territorial and monogamous, resembling the modern human social disposition. We review (i) how baseline and dynamic T levels predict and/or impact aggressive behavior and disposition; (ii) how factors related to social and physical context influence T and aggression; (iii) the reinforcing or "rewarding" aspects of aggressive behavior; and (iv) the function of T on aggression before and during a combative encounter. Included are areas that may need further research. We argue that animal studies investigating these topics fill in gaps to help paint a more complete picture of how androgenic steroids drive the output of aggressive behavior in all animals, including humans.

Social and physical environments as a source of individual variation in the rewarding effects of testosterone in male California mice (Peromyscus californicus).

Despite extensive research revealing the occurrence of testosterone (T) pulses following social encounters, it is unclear how they lead to varied behavioral responses. We investigated the influence of residency (home versus unfamiliar environment) and social/sexual experience (pair-bonded, isolated or housed with siblings) on the plasticity of T's rewarding effects by measuring the development of conditioned place preferences (CPPs), a classical paradigm used to measure the rewarding properties of drugs. For pair-bonded males, T-induced CPPs were only produced in the environment wherein the social/sexual experience was accrued and residency status had been achieved. For isolated males, the T-induced CPPs only occurred when the environment was unfamiliar. For males housed with a male sibling, the T-induced CPPs were prevented in both the home and unfamiliar chambers. Our results reveal the plasticity of T's rewarding effects, and suggest that the behavioral functions of T-pulses can vary based on social/sexual experience and the environment in which residency was established. The formation of CPPs or reward-like properties of drugs and natural compounds can therefore exhibit malleability based on past experience and the current environment.

Male fidelity expressed through rapid testosterone suppression of ultrasonic vocalizations to novel females in the monogamous California mouse.

The steroid hormone testosterone (T) is a well-known mediator of male sexual behavior in vertebrates. However, less is known about T's rapid effects on sexual behavior, particularly those involving ultrasonic vocalizations (USVs), a mode of communication that can influence mate acquisition in rodents. Using the monogamous California mouse, Peromyscus californicus, we tested whether T rapidly alters male USV production by giving T or saline injections to non-paired (sexually naïve) males and paired (paternally experienced and pair-bonded) males immediately prior to a brief exposure to an unrelated, novel female. Among non-paired males, no differences in the total number of USVs were observed; however, T increased the proportion of simple sweeps produced. Among paired males, T decreased the number of USVs produced, and this change was driven by a reduction in simple sweeps. These results suggest a differential rapid effect of T pulses between non-paired and paired males upon exposure to a novel female. Additionally, we observed a positive correlation in the production of USVs made between males and novel females, and this relationship was altered by T. Given the importance of USVs in sexual communication, our study supports an essential concept of monogamy in that mate fidelity is reinforced by decreased responsiveness to prospective mates outside of the pair bond. The central mechanism in pair bonded males that decreases their responsiveness to novel females appears to be one that T can trigger. This is among the first studies to demonstrate that T can inhibit sexually related behaviors and do so rapidly.

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

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 three-chambered 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.

Non-genomic transmission of paternal behaviour between fathers and sons in the monogamous and biparental California mouse.

Maternal behaviour has profound, long-lasting implications for the health and well-being of developing offspring. In the monogamous California mouse (Peromyscus californicus), care by both parents is critical for offspring survival. We tested the hypothesis that similar to maternal care in rodents, paternal huddling and grooming (HG) behaviour can be transmitted to future generations via behavioural mechanisms. In California mice, testosterone maintains paternal HG behaviour. In the present study, we randomly assigned a group of male California mice to castration or sham-operated conditions and allowed them to raise their offspring normally. Adult sons of these males were paired with a female, and they were observed interacting with their own offspring. We found that like their fathers, the sons of castrated males huddled and groomed their young at lower levels than the sons of sham-operated fathers. The sons of castrates also retrieved pups more frequently. When both parents were present, the sons of castrates also showed a trend towards engaging in less exploratory behaviour. These data support the hypothesis that paternal behaviour, like maternal behaviour, can be transferred to future generations via epigenetic mechanisms and suggest that in a biparental species both parents contribute to offspring behavioural development.

Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression.

Winning aggressive disputes can enhance future fighting ability and the desire to seek out additional contests. In some instances, these effects are long lasting and vary in response to the physical location of a fight. Thus, in principle, winning aggressive encounters may cause long-term and context-dependent changes to brain areas that control the output of antagonistic behavior or the motivation to fight (or both). We examined this issue in the territorial California mouse (Peromyscus californicus) because males of this species are more likely to win fights after accruing victories in their home territory but not after accruing victories in unfamiliar locations. Using immunocytochemistry and real-time quantitative PCR, we found that winning fights either at home or away increases the expression of androgen receptors (AR) in the medial anterior bed nucleus of the stria terminalis, a key brain area that controls social aggression. We also found that AR expression in brain regions that mediate motivation and reward, nucleus accumbens (NAcc) and ventral tegmental area (VTA), increases only in response to fights in the home territory. These effects of winning were likely exclusive to the neural androgenic system because they have no detectible impact on the expression of progestin receptors. Finally, we demonstrated that the observed changes in androgen sensitivity in the NAcc and VTA are positively associated with the ability to win aggressive contests. Thus, winning fights can change brain phenotype in a manner that likely promotes future victory and possibly primes neural circuits that motivate individuals to fight.

Behavioral convergence in defense behaviors in pair bonded individuals correlates with neuroendocrine receptors in the medial amygdala.

Monogamous, pair-bonded animals coordinate intra-pair behavior for spatially separated challenges including territorial defense and nest attendance. Paired California mice, a monogamous, territorial and biparental species, approach intruders together or separately, but often express behavioral convergence across intruder challenges. To gain a more systems-wide perspective of potential mechanisms contributing to behavioral convergence across two conspecific intruder challenges, we conducted an exploratory study correlating behavior and receptor mRNA (Days 10 and 17 post-pairing). We examined associations between convergence variability in pair time for intruder-oriented behaviors with a pair mRNA index for oxytocin (OXTR), androgen (AR), and estrogen alpha (ERα) receptors within the medial amygdala (MeA) and the anterior olfactory nucleus (AON), brain regions associated with social behavior. An intruder behavior index revealed a bimodal distribution of intruder-related behaviors in Challenge 1 and a unimodal distribution in Challenge 2, suggesting population behavioral convergence, but no significant correlations with neuroendocrine measures. However, OXTR, AR, and ERα mRNA in the MeA were positively associated with convergence in individual intruder-related behaviors, suggesting multiple mechanisms may influence convergence. Mice could also occupy the nest during intruder challenges and convergence in nest attendance was positively correlated with MeA OXTR. At an individual level, nest attendance was positively associated with MeA ERα. Vocalizations were positively associated with AR and ERα mRNA. No positive associations were found in the AON. Overall, neuroendocrine receptors were implicated in convergence of a monogamous pair's defense behavior, highlighting the potential importance of the MeA as part of a circuit underlying convergence.

Compatibility drives female preference and reproductive success in the monogamous California mouse (Peromyscus californicus) more strongly than male testosterone measures.

Female assessment of male attractiveness and how preferred qualities impact reproductive success is central to the study of mate choice. Male attractiveness may depend on traits beneficial to the reproductive success (RS) of any female, termed 'universal quality', and/or on behavioral and biological interactions between potential mates that reflect 'compatibility'. The steroid hormone testosterone (T) often underlies male attractiveness in rodents and is associated with enhanced paternal care in the monogamous and biparental California mouse (Peromyscus californicus). We hypothesized that (1) T-characteristics are universally attractive to female California mice and that (2) if reproductive success is higher for females mated with preferred males, then females mated with males preferred by other females will also have higher reproductive success. Alternatively, we speculated that pair compatibility, based on emergent pair qualities, is important for a species with coordinated offspring care. We assessed individual T-characteristics in three ways: (1) T-response to GnRH challenges (2) baseline T-level and (3) T-response to a female. Testosterone-response did not predict female preference, but females spent more time investigating males with higher baseline T (accounting for only 9.6% of the variation in investigation time). None of the T-measures was associated with RS. Females paired with males they preferred produced litters more quickly and had higher RS than females paired with their non-preferred males. Naïve females who did not undergo preference tests had equivalent RS regardless of whether their mate was preferred or non-preferred by another female. These data suggest that higher male T elicits investigation, but female preference in the California mouse is more strongly linked with compatibility because individual preference was a better predictor of RS than any T measure.

Naturally occurring variation in vasopressin immunoreactivity is associated with maternal behavior in female Peromyscus mice.

In many mammals, species-appropriate social behavior is necessary for an individual's ability to survive and reproduce. In the present study, we examined whether arginine-vasopressin (AVP) pathways that have been associated with social behavior differed between two closely related species of Peromyscus mice with different patterns of maternal behavior. We also tested whether individual levels of AVP-immunoreactive staining (AVP-ir) were associated with individual levels of maternal behavior as measured using a composite score consisting of huddling, nursing, grooming and time spent inside the nest (HNGI score). In addition, we examined whether these associations between vasopressin and behavior differed between species. Females from the highly biparental species, California mice, displayed higher AVP-ir in the bed nucleus of the stria terminalis (BNST), which corresponded with a higher level of nest building and a higher HNGI score than was found in the less parental white-footed mice. The HNGI score was positively associated with AVP-ir in the medial amygdala in female California mice but not white-footed mice. Finally, we examined whether AVP-ir in these pathways varied based on the species-specific rearing environments by reciprocally cross-fostering California mice and white-footed mice. In contrast to previous research with male California mice, cross-fostering itself had no effect on maternal behavior or any consistent effect on AVP-ir staining in brain areas such as the BNST and associated brain areas. This suggests that there is little plasticity in maternal behavior and that the underlying AVP system in females does not respond to the postnatal environment provided by the parents. The positive associations between maternal behavior and AVP-ir indicate that AVP may regulate maternal behavior despite the lack of plasticity in AVP and maternal behavior.

Monogamous and promiscuous rodent species exhibit discrete variation in the size of the medial prefrontal cortex.

Limbic-associated cortical areas, such as the medial prefrontal and retrosplenial cortex (mPFC and RS, respectively), are involved in the processing of emotion, motivation, and various aspects of working memory and have been implicated in mating behavior. To determine whether the independent evolution of mating systems is associated with a convergence in cortical mechanisms, we compared the size of mPFC and RS between the monogamous prairie vole (Microtus ochrogaster) and the promiscuous meadow vole (Microtus pennsylvanicus), and between the monogamous California mouse (Peromyscus californicus) and the promiscuous white-footed mouse (Peromyscus leucopus). For both promiscuous mice and voles, the mPFC occupied a significantly larger percentage of total cortex than in the monogamous species. No significant differences were observed for the RS or overall cortex size with respect to mating system, supporting the convergent evolution of mPFC size, specifically. Individual differences in the mating behavior of male prairie voles (wandering versus pair-bonding), presumably facultative tactics, were not reflected in the relative size of the mPFC, which is likely a heritable trait. Given the importance of the mPFC for complex working memory, particularly object-place and temporal order memory, we hypothesize that the relatively greater size of the mPFC in promiscuous species reflects a greater need to remember multiple individuals and the times and locations in which they have been encountered in the home range.

Intranasal oxytocin reduces pre-courtship aggression and increases paternal response in California mice (Peromyscus californicus).

Oxytocin (OXT) is a neuropeptide that can facilitate prosocial behavior and decrease social stress and anxiety but can also increase aggression in some contexts. We investigated whether acute pulses of intranasal (IN) OXT influenced social behavior during social challenges that are likely to occur throughout the lifespan of a wild mouse. To test this, we examined the acute effects of IN OXT in the male California mouse (Peromyscus californicus), a monogamous, biparental, and territorial rodent, using a within-subjects longitudinal design. Social challenges included a pre-courtship male-female encounter conducted during the (1) initial aggressive and not the following affiliative phase of courtship, (2) same-sex resident intruder test, and (3) parental care test. Consecutive tests and doses were separated by at least two weeks. Males were treated with intranasal infusions of 0.8 IU/kg OXT or saline controls 5-min before each behavioral test, receiving a total of three treatments of either IN OXT or saline control. We predicted that IN OXT would 1) decrease aggression and increase affiliation during the pre-courtship aggression phase, 2) increase aggression during resident intruder paradigms, and 3) increase paternal care and vocalizations during a paternal care test. As predicted, during pre-courtship aggression with a novel female, IN OXT males displayed less contact aggression than control males, although with no change in affiliative behavior. However, post-pairing, during the resident intruder test, IN OXT males did not differ from control males in contact aggression. During the paternal care test, IN OXT males were quicker to approach their pups than control males but did not differ in vocalizations produced, unlike our previous research demonstrating an effect on vocalizations in females. In summary, during pre-courtship aggression and the paternal care test, IN OXT reduced antisocial behavior; however, during the resident intruder test, IN OXT did not alter antisocial behavior. These data suggest that IN OXT promotes prosocial behavior specifically in social contexts that can lead to affiliation.

Testosterone pulses paired with a location induce a place preference to the nest of a monogamous mouse under field conditions.

Changing social environments such as the birth of young or aggressive encounters present a need to adjust behavior. Previous research examined how long-term changes in steroid hormones mediate these adjustments. We tested the novel concept that the rewarding effects of transient testosterone pulses (T-pulses) in males after social encounters alter their spatial distribution on a territory. In free-living monogamous California mice (Peromyscus californicus), males administered three T-injections at the nest spent more time at the nest than males treated with placebo injections. This mimics T-induced place preferences in the laboratory. Female mates of T-treated males spent less time at the nest but the pair produced more vocalizations and call types than controls. Traditionally, transient T-changes were thought to have transient behavioral effects. Our work demonstrates that in the wild, when T-pulses occur in a salient context such as a territory, the behavioral effects last days after T-levels return to baseline.

Species differences in the winner effect disappear in response to post-victory testosterone manipulations.

Evolutionary processes can interact with the mechanisms of steroid hormone action to drive interspecific variation in behavioural output, yet the exact nature of these interactions is poorly understood. To investigate this issue, we compare the endocrine machinery underlying the winner effect (an ability to increase winning behaviour in response to past victories) in two closely related species of Peromyscus mice. Typically, after winning a fight, California mice (Peromyscus californicus) experience a testosterone (T) surge that helps enhance their future winning behaviour, whereas white-footed mice (Peromyscus leucopus) experience neither a T surge nor a change in subsequent winning behaviour. However, our results indicate that when the post-victory T response of male white-footed mice is phenotypically engineered to resemble that of California mice, individuals are capable of developing a strong and lasting winner effect. Moreover, this 'induced' winner effect in white-footed mice qualitatively matches the winner effect that develops naturally in California mice. Taken together, these findings suggest that white-footed mice have the physiological machinery necessary to form a robust winner effect comparable to that formed by California mice, but are unable to endogenously activate this machinery after achieving winning experiences. We speculate that evolutionary processes, like selection, operate on the physiological substrates that govern post-victory T release to guide divergence in the winner effect between these two species.