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.     

Sexual reward in male rats: effects of sexual experience on conditioned place preferences associated with ejaculation and intromissions

Various behavioral models and studies have provided evidence suggesting that male rat sexual behavior has rewarding and reinforcing properties. However, there is little information regarding the rewarding values of the different components of sexual behavior. Therefore, this study used a conditioned place preference (CPP) paradigm to address whether ejaculation and intromissions differ in their rewarding incentive values. We also addressed whether the differential rewarding values were dependent on prior sexual experience. Sexually naïve and experienced males received one pairing of either intromissions or ejaculation with one of the chambers in the CPP box. The amount of time spent in each chamber of the CPP apparatus after conditioning was then measured. Both sexually naïve and sexually experienced males formed a CPP for ejaculation, while only sexually naïve, and not sexually experienced, males formed a CPP for intromissions. Moreover, in sexually naïve males, multiple pairings of ejaculation with the designated chamber resulted in a CPP relative to the control chamber paired with display of intromissions. These data support the hypothesis that there is a hierarchy of rewarding sexual behavior, with ejaculation being the most rewarding component, and that the rewarding incentive value of other components of sexual behavior is dependent upon prior sexual experience.     

Chemosensory Recognition of Familiar and Unfamiliar Conspecifics by the Scincid Lizard Eumeces laticeps

The ability of broad-headed skinks (Eumeces laticeps) to distinguish familiar from unfamiliar individuals of the opposite sex and themselves from other individuals of the same sex using only chemical stimuli was examined experimentally. Cloacal chemical stimuli were presented to lizards on moistened cotton swabs and numbers of tongue-flicks performed in 60 s were recorded. Males emitted significantly greater numbers of tongue-flicks in response to chemical cues from unfamiliar females than of female cagemates. Response rates of males housed with females and males housed alone to chemical stimuli from unfamiliar females did not differ. Chemical stimuli from unfamiliar males elicited significantly more tongue flicks from males than their own or deionized water, but their own stimuli elicited no more than the odourless control. Females tongue-flicked significantly more in response to cloacal chemical stimuli from unfamiliar males than from male cagemates. The findings indicate that both sexes of broad-headed skinks can discriminate between chemical stimuli of familiar and unfamiliar individuals of the opposite sex and that males can distinguish their own cloacal chemicals from those of unfamiliar males. The possible functions of these chemosensory capacities, including location of mates by scent-trailing and assessment of the presence of sexual competitors, are discussed in relation to the social behaviour of E. laticeps.     

Plastic male mating behavior evolves in response to the competitive environment*

Male reproductive phenotypes can evolve in response to the social and sexual environment. The expression of many such phenotypes may also be plastic within an individual's lifetime. For example, male Drosophila melanogaster show significantly extended mating duration following a period of exposure to conspecific male rivals. The costs and benefits of reproductive investment, and plasticity itself, can be shaped by the prevailing sociosexual environment and by resource availability. We investigated these ideas using experimental evolution lines of D. melanogaster evolving under three fixed sex ratios (high, medium, and low male‐male competition) on either rich or poor adult diets. We found that males evolving in high‐competition environments evolved longer mating durations overall. In addition, these males expressed a novel type of plastic behavioral response following exposure to rival males: they both significantly reduced and showed altered courtship delivery, and exhibited significantly longer mating latencies. Plasticity in male mating duration in response to rivals was maintained in all of the lines, suggesting that the costs of plasticity were minimal. None of the evolutionary responses tested were consistently affected by dietary resource regimes. Collectively, the results show that fixed behavioral changes and new augmentations to the repertoire of reproductive behaviors can evolve rapidly.     

Plasticity in male mating behavior modulates female life history in fruit flies

In many species, intense male-male competition for the opportunity to sire offspring has led to the evolution of selfish reproductive traits that are harmful to the females they mate with. In the fruit fly, Drosophila melanogaster, males modulate their reproductive behavior based on the perceived intensity of competition in their premating environment. Specifically, males housed with other males subsequently transfer a larger ejaculate during a longer mating compared to males housed alone. Although the potential fitness benefits to males from such plasticity are clear, its effects on females are mostly unknown. Hence, we tested the long-term consequences to females from mating with males with distinct social experiences. First, we verified that competitive experience influences male mating behavior and found that males housed with rivals subsequently have shorter mating latencies and longer mating durations. Then, we exposed females every other day for 20 days to males that were either housed alone or with rivals, and subsequently measured their fitness. We found that females mated to males housed with rivals produce more offspring early in life but fewer offspring later in life and have shorter lifespans but similar intrinsic population growth rates. These results indicate that plasticity in male mating behavior can influence female life histories by altering females’ relative allocation to early versus late investment in reproduction and survival.     

Female influences on pair formation, reproduction and male stress responses in a monogamous cavy (Galea monasteriensis)

We examined the possible existence of, and female contributions to, pair bonds, as well as the relation of social preference to mating selectivity, in a recently identified wild guinea pig, the Muenster yellow-toothed cavy (Galea monasteriensis). In Experiment 1, females housed for approximately 20 days in an apparatus in which they could choose to approach and interact with unfamiliar males typically exhibited a robust preference for one of two available males. DNA fingerprinting revealed a strong association between female choice and paternity. Experiment 2 examined the influence of the removal and return of the female on male plasma cortisol levels and behavior in established breeding pairs. A 2-h period of separation in the home enclosure elevated male cortisol levels. Return of the female to the home enclosure reduced male cortisol levels 2 h later, whereas continued separation did not. Reunion in either the home or novel enclosure increased socio-positive and courtship/sexual behavior, as well as time spent in proximity of the partner. Together, these results provide evidence for a substantial female influence on pair bond formation and maintenance in G. monasteriensis and further support for the existence of social and sexual monogamy in this species.     

Heterosexual housing increases the retention of courtship behavior following castration and elevates metabolic capacity in limbic brain nuclei in male whiptail lizards,Cnemidophorus inornatus

In male vertebrates the display of courtship behavior depends on the presence of testicular androgens. However, social experiences in adulthood can alter the hormonal dependence of courtship behavior in a variety of species, and we have previously proposed that these behavioral changes are linked to changes in neural metabolic capacity (cytochrome oxidase activity). Here we investigated the effects of prior social experience (housing with females vs housing in isolation) on the retention of courtship behavior following gonadectomy and on cytochrome oxidase (CO) activity in male little striped whiptail lizards, Cnemidophorus inornatus. In Experiment 1, we found that males that were previously housed with females (HWF males) continued to display courtship behavior longer after castration than males previously housed in isolation (ISOLATE males). This is similar to the behavioral plasticity found in rodents and cats. On the other hand, courtship behavior while gonadally intact was indistinguishable between HWF and ISOLATE males. Because all males were housed individually following castration, the difference is due to different social experiences prior to castration. In Experiment 2, we found that gonadally intact HWF males had significantly elevated CO activity in the preoptic area, amygdala, and anterior and ventromedial hypothalamic areas relative to intact ISOLATE males. No significant differences in metabolism were found in the lateral septum, lateral hypothalamus, and habenula or in hindlimb muscle, suggesting that the increase in metabolism is specific to brain nuclei involved in courtship behavior. Altogether, this demonstrates that elevations in metabolic capacity correlate with experience-dependent increases in robustness to castration.     

Phenotypic plasticity in female mate choice behavior is mediated by an interaction of direct and indirect genetic effects in Drosophila melanogaster

Female mate choice is a complex decision‐making process that involves many context‐dependent factors. In Drosophila melanogaster, a model species for the study of sexual selection, indirect genetic effects (IGEs) of general social interactions can influence female mate choice behaviors, but the potential impacts of IGEs associated with mating experiences are poorly understood. Here, we examined whether the IGEs associated with a previous mating experience had an effect on subsequent female mate choice behaviors and quantified the degree of additive genetic variation associated with this effect. Females from 21 different genetic backgrounds were housed with males from one of two distinct genetic backgrounds for either a short (3 hr) or long (48 hr) exposure period and their subsequent mate choice behaviors were scored. We found that the genetic identity of a previous mate significantly influenced a female's subsequent interest in males and preference of males. Additionally, a hemiclonal analysis revealed significant additive genetic variation associated with experience‐dependent mate choice behaviors, indicating a genotype‐by‐environment interaction for both of these parameters. We discuss the significance of these results with regard to the evolution of plasticity in female mate choice behaviors and the maintenance of variation in harmful male traits.     

Rapid steroid influences on visually guided sexual behavior in male goldfish

The ability of steroid hormones to rapidly influence cell physiology through nongenomic mechanisms raises the possibility that these molecules may play a role in the dynamic regulation of social behavior, particularly in species in which social stimuli can rapidly influence circulating steroid levels. We therefore tested if testosterone (T), which increases in male goldfish in response to sexual stimuli, can rapidly influence approach responses towards females. Injections of T stimulated approach responses towards the visual cues of females 30–45 min after the injection but did not stimulate approach responses towards stimulus males or affect general activity, indicating that the effect is stimulus-specific and not a secondary consequence of increased arousal. Estradiol produced the same effect 30–45 min and even 10–25 min after administration, and treatment with the aromatase inhibitor fadrozole blocked exogenous T's behavioral effect, indicating that T's rapid stimulation of visual approach responses depends on aromatization. We suggest that T surges induced by sexual stimuli, including preovulatory pheromones, rapidly prime males to mate by increasing sensitivity within visual pathways that guide approach responses towards females and/or by increasing the motivation to approach potential mates through actions within traditional limbic circuits.     

Is Self‐Grooming by Male Prairie Voles a Predictor of Mate Choice?

Self-grooming by mammals is a form of scent dissemination in which individuals anoint themselves with salivary, anogenital, and other body odours. Self-grooming has been proposed to be a sexually selected trait favoured in reproductive competition and sexual attraction. We tested the hypothesis that females would show a mating preference for males that self-groomed more than a reproductive competitor that groomed less. In mate-choice experiments in which females had a choice of two tethered males, non pair-bonded females did not choose males based on their frequency of self-grooming. In a second experiment in which pair-bonded females in postpartum oestrus had access to their current mate and two strange males, strange males groomed significantly more than pair-bonded mates, yet attained the fewest copulations. Non pair-bonded females and pair-bonded males and females groomed significantly less often than did non pair-bonded males. Self-grooming behaviour was consistent with the sexual attraction hypothesis, but the frequency of self-grooming did not increase a male's mating success. We conclude that the frequency and time spent self grooming are not good predictors of mating success.     

Pair-housing of male and female rats during chronic stress exposure results in gender-specific behavioral responses

Social support has a positive influence on the course of a depression and social housing of rats could provide an animal model for studying the neurobiological mechanisms of social support. Male and female rats were subjected to chronic footshock stress for 3 weeks and pair-housing of rats was used to mimic social support. Rats were isolated or housed with a partner of the opposite sex. A plastic tube was placed in each cage and subsequently used as a 'safe' area in an open field test. Time spent in the tube was used as a measurement of anxiety levels. Chronic stress increased adrenal weights in all groups, except for isolated females who showed adrenal hypertrophy in control conditions. In isolated males, chronic stress resulted in an increase in the time the animals spent in the tube. While stress did not affect this parameter in socially housed males, males with a stressed partner showed a similar response as isolated stressed males. Even though adrenal weights showed that isolated females were more affected by stress, after chronic stress exposure, they spent less time in the tube than socially housed females. Socially housed stressed females spent less time in the 'safe' tube compared to control counterparts, indicating that stress has a gender-specific behavioral effect. In conclusion: pair-housing had a stress-reducing effect on behavior in males. Isolation of females was stressful by itself. Pair housing of females was not able to prevent stress-induced behavioral changes completely, but appeared to reduce the effects of chronic stress.     

Plasticity in reproductive phenotypes reveals status-specific correlations between behavioral, morphological, and physiological sexual traits

Reproductive success is determined by a complex interplay between multiple sexual traits that promote mate acquisition and, following copulation, provide control over paternity. The intensity of sexual competition that individuals experience often fluctuates, and here we investigate how this influences the expression of reproductive traits and their relationships. We show in the fowl, Gallus gallus, that males of different social status, which experience different intensities of sexual competition, before and after copulation, have different reproductive phenotypes. Dominant males are more vigilant, feed less, and have larger sexual ornaments than subordinate males. Experimentally manipulating social status revealed that these differences were phenotypically plastic, indicating multiple sexual traits were dependent on the social environment. We integrated these data with previous published findings on changes in sperm numbers and velocity to show that relationships between traits were different for males when they were dominant and when they were subordinate. Furthermore, when males switched status a complex array of negative and positive correlations between the degree traits changed was observed. Our results suggest that variation in the intensity of sexual competition generates reversible plasticity in reproductive phenotypes and that relationships between sexual traits may be variable and influence the evolution of reproductive strategies.     

Psychobiology of sexual behavior in a whiptail lizard, Cnemidophorus inornatus

This study investigated the effects of social environment on gonadal recrudescence and sexual behavior in male and female Little Striped Whiptail lizards (Cnemidophorus inornatus). The presence of sexually active males facilitates ovarian recrudescence in conspecific females. Similarly, the presence of reproductively active females facilitates testicular recrudescence in conspecific males. Males housed with females, however, had lower average circulating concentrations of testosterone and dihydrotestosterone, and higher average concentrations of corticosterone compared to intact males housed in isolation. In other studies, the presence of reproductively active females partially restored courtship behavior in castrated males compared to castrated males housed in isolation. Despite the stimulatory effects of females on castrates, exogenous androgens are required for complete restoration of all components of sexual behavior in male C. inornatus. Females are receptive to male courtship and copulatory behavior only during the vitellogenic stages; females in previtellogenic or postovulatory ovarian stages aggressively reject male courtship advances. These findings demonstrate reciprocal effects of sexual behaviors of males and females upon each other's reproductive behavior and physiology.     

Social Change Affects Vocal Structure in a Callitrichid Primate (Callithrix kuhlii)

Vocal plasticity in the face of changing social context is well‐documented in passerine birds, but the degree to which changes in social environment affect the vocal structure of non‐human primates is a topic which has remained largely unexplored. We assessed whether modification of social environments, in this case the presence of marmosets in neighboring cages, influenced the vocal morphology of phee calls, which possess ‘signature’‐like features, in Wied's black tufted‐ear marmosets (Callithrix kuhlii). Individual phee calls were obtained over a period of 8 wk from 11 animals maintained in rooms with stable social environments. After this baseline phase, seven marmosets were housed for an additional 8 wk in rooms that contained cages with unfamiliar marmosets, while four marmosets maintained the same neighbors as the first phase. Calls were digitized and both frequency and temporal parameters were measured. Multivariate discriminant function analyses (DFA) generated from vocalizations collected in the first phase produced functions that accurately classified calls to the correct individual, showing that calls had significant individual distinctiveness. DFAs generated from vocalizations in the first phase of the study continued to show high classification accuracy for marmosets in a stable social environment, but DFAs from the first phase were significantly less likely to correctly classify vocalizations in marmosets that were housed next to novel conspecifics. These data show that phee calls, which have signature‐like properties in marmosets, can be modified by changes in social context. The results suggest a degree of plasticity in vocal signals that is rare among non‐human primates.     

The physiological and behavioral impact of sensory contact among unfamiliar adult mice in the laboratory

Housing mice in the laboratory in groups enables social interaction and is the way a laboratory should house mice. However, adult males show reciprocal aggression and are therefore frequently housed individually. Alternatively, a grid divider, which allows sensory contact by sight and smell but prevents fighting and injuries, can separate mice within 1 cage. This study examined the influence of this housing method on various physiological and behavioral parameters. Adult male mice housed for 10 days with sensory contact to an unfamiliar male displayed significant increases in heart rate (HR), body core temperature (BT), and motor activity (ACT). Furthermore, the mice suffered impaired nest-building behavior and significantly reduced body weight. Conversely, males housed in a similar manner with a female companion showed only a transient elevation of ACT, BT, and HR. Although no clear beneficial effect of housing males with sensory contact to females was evident, this study could not exclude it. On the other hand, housing of mature males in this way leads to sustained detrimental alterations of physiology and behavior, thus implying severe impairment of animal well-being.     

The effect of social environment on estrogen excretion,scent marking,and sociosexual behavior in tamarins (Saguinus oedipus)

The influence of various social environments on estrogen excretion, scent marking, and the expression of sociosexual behavior was examined in cotton-top tamarins (Sanguinus o. oedipus). Behavioral observations and urine collections were conducted on five females while first housed in their natal family group or in the presence of another cycling adult female and then while housed with an unrelated adult male in a separate cage. Behavioral observations only were conducted on males in natal family groups and while housed with an unrelated adult female. Levels of urinary estrone and estradiol for females were measured by specific radioimmunoassays. Females housed in family groups or in the presence of an adult cycling female showed low and noncyclic patterns of estrogen excretion. Removal from these environments resulted in a rapid increase in urinary estrone and estradiol and three of five females demonstrated cyclic patterns of estrone excretion. Rates of anogenital marking in females were elevated after the social change, and sexual interactions, virtually absent in the original environments, were observed in all five females. In males, similar manipulations of the social environment affected the expression of sexual behavior, but not scent marking. The social environment, therefore has a profound impact on fertility and sociosexual behavior in cotton-top tamarin groups, with implications for callitrichid social structure and behavior.     

Social isolation and the inflammatory response: sex differences in the enduring effects of a prior stressor

Numerous epidemiological studies have demonstrated an association between persistent social isolation and "all-cause" morbidity and mortality. To date, no causal mechanism for these findings has been established. Whereas animal studies have often reported short-term effects of social isolation on biological systems, the long-term effects of this adverse psychological state have been understudied. This is the first animal study to examine the effects of long-term social isolation from weaning through young adulthood on an innate inflammatory response linked to numerous disease processes. Results presented here offer a plausible link between vulnerability to disease and social neglect. For socially isolated male and female Sprague-Dawley rats, a naturally gregarious species, formation of a granuloma in response to a subcutaneous injection of carrageenin (seaweed) was significantly delayed compared with the response of animals housed in single-sex groups of five. Significant sex differences, however, emerged when an acute prior stressor was superimposed on the experience of chronic social isolation. In this context, isolated females produced a more robust inflammatory response than isolated males. This sexual dimorphism at the nexus of chronic social isolation, acute stress, and inflammatory processes may account for the observation in humans that men with low levels of social integration are more vulnerable to disease and death than women.