Sex and seasonal differences in hippocampal volume and neurogenesis in brood‐parasitic brown‐headed cowbirds (Molothrus ater)

Brown‐headed cowbirds (Molothrus ater) are one of few species in which females show more complex space use than males. Female cowbirds search for, revisit, and parasitize host nests and, in a previous study, outperformed males on an open field spatial search task. Previous research reported a female‐biased sex difference in the volume of the hippocampus, a region of the brain involved in spatial memory. Neurons produced by adult neurogenesis may be involved in the formation of new memories and replace older neurons that could cause interference in memory. We tested for sex and seasonal differences in hippocampal volume and neurogenesis of brood‐parasitic brown‐headed cowbirds and the closely related non‐brood‐parasitic red‐winged blackbird (Agelaius phoeniceus) to determine whether there were differences in the hippocampus that reflected space use in the wild. Females had a larger hippocampus than males in both species, but hippocampal neurogenesis, measured by doublecortin immunoreactivity (DCX+), was greater in female than in male cowbirds in the absence of any sex difference in blackbirds, supporting the hypothesis of hippocampal specialization in female cowbirds. Cowbirds of both sexes had a larger hippocampus with greater hippocampal DCX+ than blackbirds. Hippocampus volume remained stable between breeding conditions, but DCX+ was greater post‐breeding, indicating that old memories may be lost through hippocampal reorganization following breeding. Our results support, in part, the hypothesis that the hippocampus of cowbirds is specialized for brood parasitism. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 76: 1275–1290, 2016     

Stress experienced in utero reduces sexual dichotomies in neurogenesis, microenvironment, and cell death in the adult rat hippocampus

Hippocampal function and plasticity differ with gender, but the regulatory mechanisms underlying sex differences remain elusive and may be established early in life. The present study sought to elucidate sex differences in hippocampal plasticity under normal developmental conditions and in response to repetitive, predictable versus varied, unpredictable prenatal stress (PS). Adult male and diestrous female offspring of pregnant rats exposed to no stress (control), repetitive stress (PS-restraint), or a randomized sequence of varied stressors (PS-random) during the last week of pregnancy were examined for hippocampal proliferation, neurogenesis, cell death, and local microenvironment using endogenous markers. Regional volume was also estimated by stereology. Control animals had comparable proliferation and regional volume regardless of sex, but females had lower neurogenesis compared to males. Increased cell death and differential hippocampal precursor kinetics both appear to contribute to reduced neurogenesis in females. Reduced local interleukin-1beta (IL-1beta) immunoreactivity (IR) in females argues for a mechanistic role for the anti-apoptotic cytokine in driving sex differences in cell death. Prenatal stress significantly impacted the hippocampus, with both stress paradigms causing robust decreases in actively proliferating cells in males and females. Several other hippocampal measures were feminized in males such as precursor kinetics, IL-1beta-IR density, and cell death, reducing or abolishing some sex differences. The findings expand our understanding of the mechanisms underlying sex differences and highlight the critical role early stress can play on the balance between proliferation, neurogenesis, cell death, and hippocampal microenvironment in adulthood.     

Dysregulation of neonatal hippocampal cell genesis in the androgen insensitive Tfm rat

The first two weeks of life are a critical period for hippocampal development. At this time gonadal steroid exposure organizes sex differences in hippocampal sensitivity to activational effects of steroids, hippocampal cell morphology and hippocampus dependent behaviors. Our laboratory has characterized a robust sex difference in neonatal neurogenesis in the hippocampus that is mediated by estradiol. Here, we extend our knowledge of this sex difference by comparing the male and female hippocampus to the androgen insensitive testicular feminized mutant (Tfm) rat. In the neonatal Tfm rat hippocampus, fewer newly generated cells survive compared to males or females. This deficit in cell genesis is partially recovered with the potent androgen DHT, but is more completely recovered following estradiol administration. Tfm rats do not differ from males or females in the level of endogenous estradiol in the neonatal hippocampus, suggesting other mechanisms mediate a differential sensitivity to estradiol in male, female and Tfm hippocampus. We also demonstrate disrupted performance on a hippocampal-dependent contextual fear discrimination task. Tfm rats generalize fear across contexts, and do not exhibit significant loss of fear during extinction exposure. These results extend prior reports of exaggerated response to stress in Tfm rats, and following gonadectomy in normal male rats.     

A developmental sex difference in hippocampal neurogenesis is mediated by endogenous oestradiol

Background

Oestradiol is a steroid hormone that exerts extensive influence on brain development and is a powerful modulator of hippocampal structure and function. The hippocampus is a critical brain region regulating complex cognitive and emotional responses and is implicated in the aetiology of several mental health disorders, many of which exhibit some degree of sex difference. Many sex differences in the adult rat brain are determined by oestradiol action during a sensitive period of development. We had previously reported a sex difference in rates of cell genesis in the developing hippocampus of the laboratory rat. Males generate more new cells on average than females. The current study explored the effects of both exogenous and endogenous oestradiol on this sex difference.

Methods

New born male and female rat pups were injected with the mitotic marker 5-bromo-2-deoxyuridine (BrdU) and oestradiol or agents that antagonize oestradiol action. The effects on cell number, proliferation, differentiation and survival were assessed at several time points. Significant differences between groups were determined by two- or thee-Way ANOVA.

Results

Newborn males had higher rates of cell proliferation than females. Oestradiol treatment increased cell proliferation in neonatal females, but not males, and in the CA1 region many of these cells differentiated into neurons. The increased rate of proliferation induced by neonatal oestradiol persisted until at least 3 weeks of age, suggesting an organizational effect. Administering the aromatase inhibitor, formestane, or the oestrogen receptor antagonist, tamoxifen, significantly decreased the number of new cells in males but not females.

Conclusion

Endogenous oestradiol increased the rate of cell proliferation observed in newborn males compared to females. This sex difference in neonatal neurogenesis may have implications for adult differences in learning strategy, stress responsivity or vulnerability to damage or disease.     

Hippocampal learning,memory, and neurogenesis: Effects of sex and estrogens across the lifespan in adults

This article is part of a Special Issue “Estradiol and Cognition”.There are sex differences in hippocampus-dependent cognition and neurogenesis suggesting that sex hormones are involved. Estrogens modulate certain forms of spatial and contextual memory and neurogenesis in the adult female rodent, and to a lesser extent male, hippocampus. This review focuses on the effects of sex and estrogens on hippocampal learning, memory, and neurogenesis in the young and aged adult rodent. We discuss how factors such as the type of estrogen, duration and dose of treatment, timing of treatment, and type of memory influence the effects of estrogens on cognition and neurogenesis. We also address how reproductive experience (pregnancy and mothering) and aging interact with estrogens to modulate hippocampal cognition and neurogenesis in females. Given the evidence that adult hippocampal neurogenesis plays a role in long-term spatial memory and pattern separation, we also discuss the functional implications of regulating neurogenesis in the hippocampus.     

Contrasting effects of opposite- versus same-sex housing on hormones,behavior and neurogenesis in a eusocial mammal

Competitive interactions can have striking and enduring effects on behavior, but the mechanisms underlying this experience-induced plasticity are unclear, particularly in females. Naked mole-rat (NMR) colonies are characterized by the strictest social and reproductive hierarchy among mammals, and represent an ideal system for studies of social competition. In large matriarchal colonies, breeding is monopolized by one female and 1–3 males, with other colony members being socially subordinate and reproductively suppressed. To date, competition for breeding status has been examined in-colony, with female, but not male, aggression observed following the death/removal of established queens. To determine whether this sex difference extends to colony-founding contexts, and clarify neural and endocrine mechanisms underlying behavioral change in females competing for status, we examined neurogenesis and steroid hormone concentrations in colony-housed subordinates, and NMRs given the opportunity to transition status via pair-housing. To this end, Ki-67 and doublecortin immunoreactivity were compared in the hippocampal dentate gyrus (DG) and basolateral amygdala (BLA) of colony-housed subordinates, and subordinates housed with a same-sex (SS) or opposite-sex (OS) conspecific. Results suggest that OS pairing in eusocial mammals promotes cooperation and enhances hippocampal plasticity, while SS pairing is stressful, resulting in enhanced HPA activation and muted hippocampal neurogenesis relative to OS pairs. Data further indicate that competition for status is confined to females, with female-female housing exerting contrasting effects on hippocampal and amygdalar neurogenesis. These findings advance understanding of social stress effects on neuroplasticity and behavior, and highlight the importance of including female-dominated species in research on aggression and intrasexual competition.     

The effect of environmental harshness on neurogenesis: a large-scale comparison

Harsh environmental conditions may produce strong selection pressure on traits, such as memory, that may enhance fitness. Enhanced memory may be crucial for survival in animals that use memory to find food and, thus, particularly important in environments where food sources may be unpredictable. For example, animals that cache and later retrieve their food may exhibit enhanced spatial memory in harsh environments compared with those in mild environments. One way that selection may enhance memory is via the hippocampus, a brain region involved in spatial memory. In a previous study, we established a positive relationship between environmental severity and hippocampal morphology in food-caching black-capped chickadees (Poecile atricapillus). Here, we expanded upon this previous work to investigate the relationship between environmental harshness and neurogenesis, a process that may support hippocampal cytoarchitecture. We report a significant and positive relationship between the degree of environmental harshness across several populations over a large geographic area and (1) the total number of immature hippocampal neurons, (2) the number of immature neurons relative to the hippocampal volume, and (3) the number of immature neurons relative to the total number of hippocampal neurons. Our results suggest that hippocampal neurogenesis may play an important role in environments where increased reliance on memory for cache recovery is critical.     

Developmental Trajectories of Amygdala and Hippocampus from Infancy to Early Adulthood in Healthy Individuals

Knowledge of amygdalar and hippocampal development as they pertain to sex differences and laterality would help to understand not only brain development but also the relationship between brain volume and brain functions. However, few studies investigated development of these two regions, especially during infancy. The purpose of this study was to examine typical volumetric trajectories of amygdala and hippocampus from infancy to early adulthood by predicting sexual dimorphism and laterality. We performed a cross-sectional morphometric MRI study of amygdalar and hippocampal growth from 1 month to 25 years old, using 109 healthy individuals. The findings indicated significant non-linear age-related volume changes, especially during the first few years of life, in both the amygdala and hippocampus regardless of sex. The peak ages of amygdalar and hippocampal volumes came at the timing of preadolescence (9–11 years old). The female amygdala reached its peak age about one year and a half earlier than the male amygdala did. In addition, its rate of growth change decreased earlier in the females. Furthermore, both females and males displayed rightward laterality in the hippocampus, but only the males in the amygdala. The robust growth of the amygdala and hippocampus during infancy highlight the importance of this period for neural and functional development. The sex differences and laterality during development of these two regions suggest that sex-related factors such as sex hormones and functional laterality might affect brain development.     

Field evidence for bi-directional sex change in the polygynous gobiid fish Trimma okinawae

The social condition of bi-directional sex change in the gobiid fish Trimma okinawae was investigated at Akamizu Beach, Kagoshima, Japan. Social groups of T. okinawae usually consisted of a large male and one or more smaller females. The number of females in the group was positively correlated with male body size and groups were usually separated from each other by 1–3 m. In total, 22 instances of female-to-male sex change and three instances of male-to-female sex change were observed during the 16 months that social groups were monitored. Two individuals changed sex twice: female to male and back to female. Female-to-male sex change occurred when the male disappeared from a group. Either the largest remaining female changed sex to male or a large female from another group immigrated and changed sex to male. Larger individuals appear to benefit from becoming male because they can monopolize the breeding opportunities with several females, as reported in other protogynous fishes. Sex change from male-to-female only occurred when a solitary male joined another group as a subordinate. Mortality rates are high in these small fish, therefore joining another group and reproducing as a female is likely to increase the reproductive value of a solitary male.     

Testosterone propionate administration prevents the loss of neurons within the central part of the medial peroptic nucleus

In the rat, the central part of the medial preoptic nucleus (MPNc) of the male is larger in volume and has a greater number of neurons than that of the female. The nucleus of the female, however, can be “sex reversed” by exposing the rat to gonadal steroids perinatally. The purpose of the present study was to examine the development of the MPNc to determine when the sex difference first appears and whether this difference occurs due to the relative accumulation of neurons into the compact part of the MPNc of the male and sex-reversed female rat or to the loss of MPNc neurons in the control female. Pregnant, female Sprague-Dawley rats were given an injection of [³H]methyl thymidine on embryonic day 18 (E18). Rats were exposed to testosterone propionate (TP) or vehicle from E20 to postnatal day 10 (PN10) or until the time of sacrifice. Pups from three groups [males (oil), females (oil), and sex-reversed females (TP)] were sacrificed on PN2, PN4, PN7, PN10, or PN30. The volume of the compact part of the MPNc increased in males and sex-reversed females after PN4 but the volume in the nucleus of females remained relatively constant. The number of neurons and [³H]thymidine-labeled cells remained elevated from PN2–PN30 in males or sex-reversed females but decreased dramatically in oiltreated females between PN4 and PN7, reaching a minimal number by PN10. Cell cross-sectional area increased with age while cell density decreased. These observations are consistent with the hypothesis that the lack of growth of the compact part of the MPNc of the female is due to a loss of neurons while the increase in volume of the male's nucleus is due at least in part to growth of its constituent neurons. © 1993 John Wiley & Sons, Inc.     

江西鄱阳湖流域中华秋沙鸭越冬期间的集群特征

2010年11月—2011年3月,采用样线法对江西鄱阳湖流域8个河段的中华秋沙鸭Mergus squamatus的集群特征进行了研究。中华秋沙鸭的集群类型包括雄性群、雌性群、混合群、雌性孤鸭和雄性孤鸭5种类型。越冬期间共记录到89群次,432只次中华秋沙鸭。其中,混合群是最多的一种集群方式,孤鸭也是越冬期间出现频次较高的一种特殊的集群方式。集群类型存在时间变化(P<0.01)。混合群中,大多数群体中雌性个体数多于雄性个体或者是一雌一雄。89群次中,孤鸭和2—8只群占总群数的87.64%,提示中华秋沙鸭主要以集小群分散活动。中华秋沙鸭越冬期间的群体大小是(4.85±4.97)只/群。不同集群类型的群体大小差异较大。集群大小可能与采砂、捕鱼、食物的丰富度等环境因子有关。调查结果显示,中华秋沙鸭越冬期间的性比是1∶0.74(n=432)。中华秋沙鸭群体大小与性比有一定的关系。     

Kinship alters the effects of forced cohabitation on body weight,mate choice and fitness in the rat-like hamster Tscheskia triton

It has been documented that social isolation imparts deleterious effects on gregarious rodents species,but caging in group imparts such effects on solitary rodents. This study was attempted at examining how kinship to affect body weight,behavioral interaction,mate choice and fitness when we caged male and female rat-like hamsters Tscheskia triton in pair,a solitary species. We found that females paired with nonsibling males became heavier than the females paired with sibling males,but both agonistic and amicable behavior between paired males and females did not differ between sibling and nonsibling groups. This indicated that kinship might reduce females' obesity in response to forced cohabitation,and dissociation might exist between physiological and behavioral responses. Furthermore,binary choice tests revealed that social familiarity between either siblings or nonsiblings decreased their investigating time spent in opposite sex conspecific of cage mates and/or their scents as compared with those of nonmates,suggesting effects of social association on mate and kin selection of the hamsters. On the other side,both females and males caged in pair with siblings show a preference between unfamiliar siblings or their scents and the counterparts of nonsiblings after two month separation,indicating that the kin recognition of the hamsters might also rely on phenotype matching. In addition,cohabitation (or permanent presence of fathers) elicited a lower survival of pups in nonsibling pairs than sibling pairs,but did not affect litter size,suggesting that kinship affects fitness when housing male and female ratlike hamsters together. Therefore,inbreeding might be adapted for rare and endangered animals.     

The effects of male harassment on mating duration in the seed bug,Togo hemipterus

Harassment on mating pairs by solitary males is usually considered an attempt by the male to (1) take over the female, (2) guard the female against further insemination (when the solitary male has previously copulated with this female), or (3) influence mating duration. Paired males of a seed bug repel harassment on mating pairs by solitary males by firmly grasping females using their legs and/or genital claspers; in this way, mating duration is prolonged. Male fertilization success increases as mating duration increases. Males of the seed bug, Togo hemipterus (Scott) (Heteroptera: Lygaeidae), use seminal substances to inhibit female remating. These substances induce protracted female refractory periods and are transferred to the females in a time‐dependent manner. Consequently, mating duration has important effects on fitness in this species. We observed harassment on T. hemipterus mating pairs by solitary males, and examined conflicts between paired and solitary males over mating duration. None of the solitary males were able to take over a mating female, and this may be due to the unique male genital structure in this species. All conflicts over mating duration resulted in wins by the paired males over the solitary males. Paired males prolonged mating durations, whereas severe harassment on mating pairs by solitary males shortened durations. We show that even though there is no immediate reward for the solitary male (i.e., it is unable to take over the mating female), this harassment behavior may be adaptive.     

Indirect female choice mediated by sex pheromones in the hermit crab Pagurus filholi

Males of the hermit crab Pagurus filholi perform precopulatory guarding behavior, and solitary males often show aggressive behavior to take away guarded females. Males behave coercively while guarding females, so direct mate choice by females seems difficult in such a situation. By performing several experiments we examined possible indirect female choice of hermit crab. Males were attached to a shell by their left cheliped to look like guarding pairs (fake guarding pairs). The shells were filled with cotton containing either seawater or pheromone water. The fake guarding pair with only seawater caused male–male combat in 60% of trials whereas with pheromone water combats occurred in 88% of trials. Mean duration of male–male combat was significantly longer in trials with drops of seawater containing pheromones than in those without pheromones. These results suggest guarding pairs themselves cause male–male combat by visual stimulation, that female sex pheromones have further significant function in the recognition of guarding pairs and intensification of male–male combat, and that females release sex pheromones while they are guarded. As a result of the combat, the larger male ended up guarding a female. This strongly suggests that females choose males indirectly by exploiting male–male competition induced by sex pheromones under male coercive behavior.     

Opposite Effects of Early Maternal Deprivation on Neurogenesis in Male versus Female Rats

Background

Major depression is more prevalent in women than in men. The underlying neurobiological mechanisms are not well understood, but recent data shows that hippocampal volume reductions in depressed women occur only when depression is preceded by an early life stressor. This underlines the potential importance of early life stress, at least in women, for the vulnerability to develop depression. Perinatal stress exposure in rodents affects critical periods of brain development that persistently alter structural, emotional and neuroendocrine parameters in adult offspring. Moreover, stress inhibits adult hippocampal neurogenesis, a form of structural plasticity that has been implicated a.o. in antidepressant action and is highly abundant early postnatally. We here tested the hypothesis that early life stress differentially affects hippocampal structural plasticity in female versus male offspring.

Principal Findings

We show that 24 h of maternal deprivation (MD) at PND3 affects hippocampal structural plasticity at PND21 in a sex-dependent manner. Neurogenesis was significantly increased in male but decreased in female offspring after MD. Since no other structural changes were found in granule cell layer volume, newborn cell survival or proliferation rate, astrocyte number or gliogenesis, this indicates that MD elicits specific changes in subsets of differentiating cells and differentially affects immature neurons. The MD induced sex-specific effects on neurogenesis cannot be explained by differences in maternal care.

Conclusions

Our data shows that early environment has a critical influence on establishing sex differences in neural plasticity and supports the concept that the setpoint for neurogenesis may be determined during perinatal life. It is tempting to speculate that a reduced level of neurogenesis, secondary to early stress exposure, may contribute to maladaptation of the HPA axis and possibly to the increased vulnerability of women to stress-related disorders.     

Social Relationships Among Male <Emphasis Type="Italic">Alouatta pigra</Emphasis>

We investigated male social relationships in 2 groups of black howlers (Alouatta pigra) in Palenque National Park, Mexico, over a 14-mo study characterized by frequent changes in male group membership. Both single males and pairs of males entered our focal groups. Single males tended to join groups, whereas pairs of males entering groups together successfully evicted resident males. The 19 male dyads across the 11 periods defined by changes in group membership were rarely in close proximity or interacting with one another. Nevertheless, 1 male formed significantly closer associations with resident females in 6 periods and achieved higher mating success during 4 of the periods when ≥1 female was sexually active. In the other 5 periods, no particular male maintained significantly closer associations with resident females, which may be a result of the rapid sequence of changes in male membership and corresponding social instability. Resident males participated frequently and consistently in mutual howling, but the resident male with the strongest female associations and highest mating success initiated howling bouts more frequently in all but 1 of the 6 socially stable periods. Though still preliminary, our findings suggest that variation in social relationships among male black howlers may be more related to their ability to establish strong relationships with females than to their relationships with one another.     

保加利亚北部地区匈牙利小家鼠的空间组织结构

本文研究了保加利亚北部地区的匈牙利小家鼠在繁殖期的空间关系和分布。这种动物最普遍的空间关系是一雄一雌,也观察到两个或三个雄鼠与一个雌鼠、一个雄鼠与两个或三个雌鼠的组织形式。很少观察到雌性的社群小组。雌鼠之间的巢区没有发现重叠。一般雄鼠的巢区大于雌鼠。有一半雄鼠的巢区与一个雌鼠的巢区相重叠,其他的雄鼠与两个成年雌鼠的巢区相重叠。这些结果表明,匈牙利小家鼠具有多变的社群繁殖婚配体制,即单配制和多配制共存。比较普遍的一雄一雌的配对形式和雌性的独居特性,以及雌性之间巢区的相对独立性,表明单配制是该物种的主要婚配体制。     

Experimental field studies of Asian ape social systems

The Asian apes, orangutans and gibbons, possess unusual social systems among anthropoid primates. Social groups of gibbons consist of mated adult pairs and their offspring; mature orangutans are primarily solitary. Recent experimental field research has begun to yield insights into the behavioral mechanisms employed by these animals to maintain their characteristic patterns of social dispersion. While spatial separation between female orangutans appears to be maintained passively, aggression, which is manifest during direct encounters and long-distance vocal interactions, mediates male asociality. Male-male aggression is the result of intense intrasexual competition occurring between animals for mating access to females. To reduce intrasexual competition, male orangutans have adopted alternative mating tactics. In contrast to female orangutans, female gibbons show marked agonistic tendencies toward conspecifics. Female territoriality contributes to preventing males from becoming polygynous. Male gibbons, restricted to monogamous relationships, attempt to ensure their paternity through intrasexual aggression. These observations suggest that the spatial dispersion of females constrains male mating options in both species. However, variations between orangutan and gibbon social systems can be understood as consequences of the temporal dispersion of sexually receptive females. The temporal clumping of females, due to relatively high operational sex ratios, limits the ability of male gibbons to acquire multiple mates. Conversely, an extremely low operational sex ratio in orangutans creates a strong selection pressure for intrasexual competition and polygamous mating. These considerations provide a novel framework for interpreting the social systems of the African apes.     

Female response to predation risk alters conspecific male behaviour during pre‐copulatory mate guarding

Mating behaviour often increases predation risk, but the vulnerability within mating pairs differs between the sexes. Such a sex difference is expected to lead to differences in responses to predation risk between the sexes. In the two‐spotted spider mite Tetranychus urticae, males engage in pre‐copulatory mate guarding because only the first mating results in fertilisation. We investigated (i) whether pre‐copulatory pairs are more conspicuous to the predatory mite Phytoseiulus persimilis than solitary females, (ii) whether the vulnerability to the predator differs between sexes within the pre‐copulatory pair, (iii) whether each sex of T. urticae responds to predation risk during pre‐copulatory mate guarding and (iv) whether T. urticae's response to predation risk affects predator behaviour. Because T. urticae females are immobile during pre‐copulatory mate guarding, we observed male behaviour to evaluate effects of predation risk. We found that the predators detect more pre‐copulatory pairs than solitary females and that more females than males of the pre‐copulatory pairs are preyed upon by the predators. The preference of spider mite males for pre‐copulatory pairs versus solitary females was affected by whether or not the female had been exposed to predators during development. Male T. urticae exposed to predation risk did not alter their behaviour. These results suggest that only the most vulnerable sex, that is the female, responds to predation risk, which modifies male behaviour. Regardless of T. urticae females’ experience, however, P. persimilis detected more T. urticae pre‐copulatory pairs than solitary females, suggesting that pre‐copulatory mate guarding itself is dangerous for T. urticae females when these predators are present. We discuss our results in the context of sex‐dependent differences in predation risk.