Teleost fishes show an extraordinary diversity of sexual patterns, social structures, and sociosexual behaviors. Sex steroid hormones are key modulators of social behaviors in teleosts as in other vertebrates and act on sex steroid receptor-containing brain nuclei that form the evolutionarily conserved vertebrate social behavior network (SBN). Fishes also display important differences relative to tetrapod vertebrates that make them particularly well-suited to study the physiological mechanisms modulating social behavior. Specifically, fishes exhibit high levels of brain aromatization and have what has been proposed to be a lifelong, steroid hormone dependent plasticity in the neural substrates mediating sociosexual behavior. In this review, we examine how estrogenic signaling modulates sociosexual behaviors in teleosts with a particular focus on agonistic behavior. Estrogens have been shown to mediate agonistic behaviors in a broad range of fishes, from sexually monomorphic gonochoristic species to highly dimorphic sex changers with alternate reproductive phenotypes. These similarities across such diverse taxa contribute to a growing body of evidence that estrogens play a crucial role in the modulation of aggression in vertebrates. As analytical techniques and genomic tools rapidly advance, methods such as LC-MS/MS, snRNAseq, and CRISPR-based mutagenesis show great promise to further elucidate the mechanistic basis of estrogenic effects on social behavior in the diverse teleost lineage.

The prairie vole (Microtus ochrogaster) is a socially monogamous rodent that establishes an enduring pair bond after cohabitation, with (6 h) or without (24 h) mating. Previously, we reported that social interaction and mating increased cell proliferation and differentiation to neuronal fate in neurogenic niches in male voles. We hypothesized that neurogenesis may be a neural plasticity mechanism involved in mating-induced pair bond formation. Here, we evaluated the differentiation potential of neural progenitor cells (NPCs) isolated from the subventricular zone (SVZ) of both female and male adult voles as a function of sociosexual experience. Animals were assigned to one of the following groups: (1) control (Co), sexually naive female and male voles that had no contact with another vole of the opposite sex; (2) social exposure (SE), males and females exposed to olfactory, auditory, and visual stimuli from a vole of the opposite sex, but without physical contact; and (3) social cohabitation with mating (SCM), male and female voles copulating to induce pair bonding formation. Subsequently, the NPCs were isolated from the SVZ, maintained, and supplemented with growth factors to form neurospheres in vitro.
Notably, we detected in SE and SCM voles, a higher proliferation of neurosphere-derived Nestin + cells, as well as an increase in mature neurons (MAP2 +) and a decrease in glial (GFAP +) differentiated cells with some sex differences. These data suggest that when voles are exposed to sociosexual experiences that induce pair bonding, undifferentiated cells of the SVZ acquire a commitment to a neuronal lineage, and the determined potential of the neurosphere is conserved despite adaptations under in vitro conditions. Finally, we repeated the culture to obtain neurospheres under treatments with different hormones and factors (brain-derived neurotrophic factor, estradiol, prolactin, oxytocin, and progesterone); the ability of SVZ-isolated cells to generate neurospheres and differentiate in vitro into neurons or glial lineages in response to hormones or factors is also dependent on sex and sociosexual context.
Social interactions that promote pair bonding in voles change the properties of cells isolated from the SVZ. Thus, SE or SCM induces a bias in the differentiation potential in both sexes, while SE is sufficient to promote proliferation in SVZ-isolated cells from male brains. In females, proliferation increases when mating is performed. The next question is whether the rise in proliferation and neurogenesis of cells from the SVZ are plastic processes essential for establishing, enhancing, maintaining, or accelerating pair bond formation. Highlights 1. Sociosexual experiences that promote pair bonding (social exposure and social cohabitation with mating) induce changes in the properties of neural stem/progenitor cells isolated from the SVZ in adult prairie voles. 2. Social interactions lead to increased proliferation and induce a bias in the differentiation potential of SVZ-isolated cells in both male and female voles. 3. The differentiation potential of SVZ-isolated cells is conserved under in vitro conditions, suggesting a commitment to a neuronal lineage under a sociosexual context. 4. Hormonal and growth factors treatments (brain-derived neurotrophic factor, estradiol, prolactin, oxytocin, and progesterone) affect the generation and differentiation of neurospheres, with dependencies on sex and sociosexual context. 5. Proliferation and neurogenesis in the SVZ may play a crucial role in establishing, enhancing, maintaining, or accelerating pair bond formation.
In this study, researchers evaluated whether social interactions and copulation induce changes in the proliferation and differentiation of neural progenitor cells in adult male and female voles using an in vitro neurosphere formation assay. The following groups were assigned: control animals without any exposure to another vole outside their litter, another group with social exposure consisting of sensory exposure to a vole of the opposite sex and a third group with social cohabitation and copulation. Forty eight hours after social interactions, cells were isolated from the neurogenic niche subventricular zone (SVZ) and cultured to assess their self-renewal and proliferation abilities to form neurospheres. The results showed in the social interaction groups, a greater number and growth of neurospheres in both males and females. Differentiation capacity was assessed by immunodetection of MAP2 and GFAP to identify neurons or glia, respectively, arise from neurospheres, with an increase in neuronal fate in groups with social interaction. In the second part of the study, the researchers analyzed the effect of different hormone and growth factor treatments and found that the response in both proliferation and differentiation potential may vary depending on the sociosexual context or sex. This study suggests that social interactions leading to pair bond formation alter the properties of SVZ cells, whereby proliferation and neurogenesis may have an impact on the establishment and maintenance of pair bonding.

Acoustic cues play a major role in social interactions in many animal species. In addition to the semantic contents of human speech, voice attributes - e.g., voice pitch, formant position, formant dispersion, etc. - have been proposed to provide critical information for the assessment of potential rivals and mates. However, prior studies exploring the association of acoustic attributes with reproductive success, or some of its proxies, have produced mixed results. Here, we investigate whether the mean fundamental frequency (F0), formant position (Pf), and formant dispersion (Df) - dimorphic attributes of the human voice - are related to sociosexuality, as measured by the Revised Sociosexual Orientation Inventory (SOI-R) - a trait also known to exhibit sex differences - in a sample of native Spanish-speaking students (101 males, 147 females). Analyses showed a significant negative correlation between F0 and sociosexual behavior, and between Pf and sociosexual desire in males but not in females. These correlations remained significant after correcting for false discovery rate (FDR) and controlling for age, a potential confounding variable. Our results are consistent with a role of F0 and Pf serving as cues in the mating domain in males but not in females. Alternatively, the association of voice attributes and sociosexual orientation might stem from the parallel effect of male sex hormones both on the male brain and the anatomical structures involved in voice production.

Impairments in social and cognitive function are a common consequence of pediatric traumatic brain injury (TBI). Rehabilitation has the potential to promote optimal behavioral recovery. Here, we evaluated whether an enhanced social and/or cognitive environment could improve long-term outcomes in a preclinical model of pediatric TBI. Male C57Bl/6 J mice received a moderately-severe TBI or sham procedure at postnatal day 21. After one week, mice were randomized to different social conditions (minimal socialization, n = 2/cage; or social grouping, n = 6/cage), and housing conditions (standard cage, or environmental enrichment (EE), incorporating sensory, motor, and cognitive stimuli). After 8 weeks, neurobehavioral outcomes were assessed, followed by post-mortem neuropathology. We found that TBI mice exhibited hyperactivity, spatial memory deficits, reduced anxiety-like behavior, and reduced sensorimotor performance compared to age-matched sham controls. Pro-social and sociosexual behaviors were also reduced in TBI mice. EE increased sensorimotor performance, and the duration of sociosexual interactions. Conversely, social housing reduced hyperactivity and altered anxiety-like behavior in TBI mice, and reduced same-sex social investigation. TBI mice showed impaired spatial memory retention, except for TBI mice exposed to both EE and group housing. In the brain, while TBI led to significant regional tissue atrophy, social housing had modest neuroprotective effects on hippocampal volumes, neurogenesis, and oligodendrocyte progenitor numbers. In conclusion, manipulation of the post-injury environment has benefit for chronic behavioral outcomes, but the benefits are specific to the type of enrichment available. This study improves understanding of modifiable factors that may be harnessed to optimize long-term outcomes for survivors of early-life TBI.

Estrogenic signaling is an important focus in studies of gonadal and brain sexual differentiation in fishes and vertebrates generally. This study examined variation in estrogenic signaling (1) across three sexual phenotypes (female, female-mimic initial phase [IP] male, and terminal phase [TP] male), (2) during socially-controlled female-to-male sex change, and (3) during tidally-driven spawning cycles in the protogynous bluehead wrasse (Thalassoma bifasciatum). We analyzed relative abundances of messenger RNAs (mRNAs) for the brain form of aromatase (cyp19a1b) and the three nuclear estrogen receptors (ER) (ERα, ERβa, and ERβb) by qPCR. Consistent with previous reports, forebrain/midbrain cyp19a1b was highest in females, significantly lower in TP males, and lowest in IP males. By contrast, ERα and ERβb mRNA abundances were highest in TP males and increased during sex change. ERβa mRNA did not vary significantly. Across the tidally-driven spawning cycle, cyp19a1b abundances were higher in females than TP males. Interestingly, cyp19a1b levels were higher in TP males close (~1 h) to the daily spawning period when sexual and aggressive behaviors rise than males far from spawning (~10-12 h). Together with earlier findings, our results suggest alterations in neural estrogen signaling are key regulators of socially-controlled sex change and sexual phenotype differences. Additionally, these patterns suggest TP male-typical sociosexual behaviors may depend on intermediate rather than low estrogenic signaling. We discuss these results and the possibility that an inverted-U shaped relationship between neural estrogen and male-typical behaviors is more common than presently appreciated.

Although medroxyprogesterone acetate (MPA) is used commonly as a contraceptive in women and female non-human primates, its effects on social behavior remain unclear. This study examined whether MPA treatment and introduction of new adult males during the breeding season influence the social behaviors of group-housed adult female rhesus macaques.
Subjects were 12 MPA-treated and 12 matched case-control females. Aggressive, affiliative, and sexual behaviors were measured.
MPA-treated females showed less affiliative and sexual behavior compared to matched controls during the breeding season. MPA treatment was associated with decreased aggression emitted toward and received from females during the breeding season.
MPA treatment is associated with differences in social behavior of female rhesus macaques during the breeding season, when normal hormonal cycles are attenuated by the treatment, but there is no indication that MPA-treated females bring an additional risk for more aggression during the male introduction and breeding season.

Gonadally intact female rats display sexual behaviors only during a portion of the estrus cycle. In standard experimental setups, the on- and offset of sexual behavior is gradual. However, in naturalistic settings, it is almost instantaneous. We assessed the changes in sociosexual behaviors at the beginning and end of behavioral estrus in ovariectomized females treated with ovarian hormones. Rats were housed in a seminatural environment, in groups of three males and four females. We scored female and male behavior during the 8 min preceding and following the first and last lordosis of behavioral estrus. Immediately before the first lordosis, there was a sharp increase in female paracopulatory behaviors whereas the end of estrus was marked by a sudden decrease in these behaviors. There was no systematic change in other female behavior patterns. These data suggest that the display of female paracopulatory behaviors plays a key role. Both during transition into and out of behavioral estrus, most behavioral changes occurred within one minute. The rapid changes must be unrelated to ovarian hormone fluctuations in these ovariectomized females. Perhaps they can be explained in terms of hormone-induced, dynamic (chaotic) changes in the function of critical structures within the brain.

The effect of various social environments on sociosexual behavior was examined in six young female cotton-top tamarins (Saguinus oedipus oedipus) and in three established breeding females. Behavioral observations and hormonal samples were collected on young females while they were living with their families, when they were isolated from conspecifics, and after they were paired with an unrelated male. While living with the family, all females showed a suppression of fertility and low frequencies of sociosexual behavior. Following removal from the family, isolated females displayed an increase in rate of scent marking and an increase in hormonal levels. When young females were paired with males, they were exposed to scent secretions from their natal families, from an unfamilar family, and from a control for a total of 24 weeks. After pairing, hormonal levels increased dramatically, and ovarian cyclicity began. An increase in sociosexual behavior and elevated levels of scent marking accompanied this physiological change. Newly paired females had higher rates of affiliative behavior and scent marking than did established breeding females. However, both newly paired and established breeding males were more likely to initiate contact, grooming bouts, and social sniffing than were females. Time to first ovulation was later in females who were exposed to scent secretions from their natal families than it was in those females given a control for the first 8 weeks following pairing. No female conceived during exposure to scent secretions. However, once normal ovarian cycling had begun or a pregnancy was established, exposure to scent secretions had no effect. Thus, the social environment influences the fertility, sociosexual behavior, and pair bond formation of cotton-top tamarins. In addition, chemical stimuli found in the scent secretions produced by the natal family are most likely involved in reproductive suppression.

Behavioral observations were made on thirteen female and seven male adult group-living chimpanzees (Pan troglodytes). The behavioral data were analyzed as a function of the day of the females\' menstrual cycles to explore the possible interrelationship between genital swelling and sociosexual behavior of female chimpanzees. Copulatory behavior was confined almost entirely to the period of genital swelling and the occurrence of male-to-female genital inspection (both female- and male-initiated) was negatively correlated with the days from swelling onset, i.e., as the presumed day of ovulation approached, genital inspection decreased, while copulatory behavior increased. In addition, more females groomed their male cagemates during the luteal phase than in the follicular phase of their cycles, whereas male-to-female grooming was positively correlated with the progress of the cycle, with peaks during the time of swelling onset and menstruation. The profile of sociosexual behavior observed throughout the menstrual cycle suggested that, although chimpanzees exhibit an extended period of sexual receptivity and genital swelling, the presumed fertile period is not concealed. The role of genital swelling in chimpanzees is discussed in relation to the possible hormonal effect on female sexuality and the evolution of chimpanzee mating strategies. © 1992 Wiley-Liss, Inc.

This study examined changes in the behavioral and hormonal patterns of cooperatively breeding pairs in a primate species with the passing of time and with specific reproductive events. We (1) compared patterns of sexual, agonistic, and affiliative behavior of newly paired pygmy marmosets with the same behavioral patterns immediately after the birth of their first set of infants; (2) determined if postpartum behavioral differences existed between pairs whose infants lived and those whose infants died; and (3) examined whether behavioral patterns changed over the course of ovarian cycles in parous pygmy marmosets as had been documented in nulliparous pairs. The behavior of pairs was recorded during daily half-hour focal samples for 60 days after pairing, and 30 or 60 days after the birth of infants for pairs whose litters died or lived, respectively. Daily urine samples from females during the study were analyzed for luteinizing hormone and pregnanediol glucuronide concentrations to determine dates of ovulation. The results indicated that males consistently altered their sexual behavior and olfactory monitoring of mates during periovulatory periods in the females\' cycles both postpairing and postpartum, while similar rates of social and sexual behavior were maintained between the conditions. Sexual behavior occurred throughout the females\' ovarian cycles. Peaks in sexual behavior during the periovulatory period in nulliparous pairs disappeared after the birth of infants. Pairs whose infants died showed higher rates of sexual behavior than pairs with surviving infants. Social and sexual behavior may function to maintain the relationship both during and outside of ovulation, especially with the loss of infants. © 1996 Wiley-Liss, Inc.