Global taxonomic and functional patterns in invertebrate assemblages from rocky-intertidal mussel beds.

Mussels form extensive beds in rocky intertidal habitats on temperate seashores worldwide. They are foundation species because their beds host many invertebrates. Mussels and their associated species differ taxonomically among biogeographic regions, but all mussel beds exhibit similar structural and functional properties. Therefore, we investigated if rocky-intertidal mussel beds from around the globe host associated communities that are functionally similar despite their underlying taxonomic differences. We gathered datasets on the abundance of invertebrates found in rocky-intertidal mussel beds from the eastern and western boundaries of the Pacific and Atlantic Oceans from both hemispheres and, then, we compared their taxonomic and functional properties. Taxonomic composition differed markedly among coasts when analyzed at the taxonomic resolution reported by the surveys (often species). However, taxonomic groups with similar ecologies (28 groups including barnacles, decapods, gastropods, polychaetes, etc.) were more universally present in mussel beds. Concomitantly, functional categories of trophic level, body type, and mobility were almost always present on all studied coasts. These taxonomic groups and trait categories, however, showed regional patterns based on their relative abundances. Overall, the ability of mussel beds to host a core community type based on taxonomic groups and functional traits emphasizes their importance for biodiversity and community functioning, making them critical organisms to preserve.

Preclinical methodological approaches investigating of the effects of alcohol on perinatal and adolescent neurodevelopment.

Despite much evidence of its economic and social costs, alcohol use continues to increase. Much remains to be known as to the effects of alcohol on neurodevelopment across the lifespan and in both sexes. We provide a comprehensive overview of the methodological approaches to ethanol administration when using animal models (primarily rodent models) and their translational relevance, as well as some of the advantages and disadvantages of each approach. Special consideration is given to early developmental periods (prenatal through adolescence), as well as to the types of research questions that are best addressed by specific methodologies. The zebrafish is used increasingly in alcohol research, and how to use this model effectively as a preclinical model is reviewed as well.

Maternal care-related differences in males and females rats' sensitivity to ethanol and the associations between the GABAergic system and steroids in males.

This study investigated the effect of maternal care on adolescent ethanol consumption, sensitivity to ethanol-induced hypnosis, as well as gonadal hormones and γ-aminobutyric acid type-A (GABAA ) systems. Long Evans rat dams were categorized by maternal licking/grooming (LG) frequency into High- and Low-LG mothers. Both female and male offspring from Low-LG rats demonstrated a greater sensitivity to ethanol-induced hypnosis in the loss-of-righting-reflex test at ethanol doses of 3.0 and 3.5 g/kg during late-adolescence (postnatal Day 50) but not at mid-adolescence (postnatal Day 42). However, we found no effect of maternal care on consumption of a 5% ethanol solution in a two-bottle choice test. We further investigated the association between the observed variations in sensitivity to ethanol-induced hypnosis and baseline hormonal levels in males. In male offspring from Low-LG mothers compared to High-LG mothers, baseline plasma corticosterone and progesterone levels were higher. GABAA α1 and δ subunit expressions were also higher in the cerebral cortex of Low-LG males but lower in the cerebellar synaptosomal fraction. Early environmental influences on adolescent sensitivity to ethanol-induced hypnosis, consumption, and preference may be mediated by gonadal hormones and possibly through GABAergic functions.

Strain-specific programming of prenatal ethanol exposure across generations.

Behavioral consequences of prenatal alcohol exposure (PAE) can be transmitted from in utero-exposed F1 generation to their F2 offspring. This type of transmission is modulated by genetic and epigenetic mechanisms. This study investigated the intergenerational consequences of prenatal exposure to a low ethanol dose (1 g/kg) during gestational days 17-20, on ethanol-induced hypnosis in adolescent male F1 and F2 generations, in two strains of rats. Adolescent Long-Evans and Sprague-Dawley male rats were tested for sensitivity to ethanol-induced hypnosis at a 3.5-g/kg or 4.5-g/kg ethanol dose using the loss of righting reflex (LORR) paradigm. We hypothesized that PAE would attenuate sensitivity to ethanol-induced hypnosis in the ethanol-exposed animals in these two strains and in both generations. Interestingly, we only found this effect in Sprague-Dawley rats. Lastly, we investigated PAE related changes in expression of GABAA receptor α1, α4, and δ subunits in the cerebral cortex of the PAE sensitive Sprague-Dawley strain. We hypothesized a reduction in the cerebral cortex GABAA receptor subunits' expression in the F1 and F2 PAE groups compared to control animals. GABAA receptor α1, α4, and δ subunits protein expressions were quantified in the cerebral cortex of F1 and F2 male adolescents by western blotting. PAE did not alter cerebral cortical GABAA receptor subunit expressions in the F1 generation, but it decreased GABAA receptor α4 and δ subunits' expressions in the F2 generation, and had a tendency to decrease α1 subunit expression. We also found correlations between some of the subunits in both generations. These strain-dependent vulnerabilities to ethanol sensitivity, and intergenerational PAE-mediated changes in sensitivity to alcohol indicate that genetic and epigenetic factors interact to determine the outcomes of PAE animals and their offspring.

Maternal care and affective behavior in female offspring: Implication of the neurosteroid/GABAergic system.

In female rats, the proestrus phase of the estrous cycle is associated with decreased levels of anxiety-like and depressive-like behavior relative to the metestrus phase. Progesterone likely modulate these behaviors, in part through the influence of its metabolite, allopregnanolone (THP) on hippocampal GABAAR subunit expression. As natural variations in maternal care have been found to influence both progesterone levels at proestrus and anxiety-like behavior in female offspring, we sought to investigate the importance of maternal care and the estrous cycle on affective behavior in female rats that had received Low or High levels of licking/grooming (LG) during early life. Subjects were tested for anxiety-like behavior in the elevated plus maze at proestrus or metestrus or for estrous cycle-dependent changes in depressive-like anhedonic behavior with a saccharin preference test. GABAAR subunit expression, and THP levels in the dorsal hippocampus and in plasma were also evaluated. Estrous cycle phase influenced saccharine preference and hippocampal THP level in both phenotypes. Low LG animals showed higher levels of hedonic behavior and anxiety-like behavior, irrespective of estrous cycle phase, as well as lower THP levels within the dorsal hippocampus when compared to High LG animals. Only High LG animals showed positive correlations between hippocampal THP levels and GABAAR subunit expression, suggesting a relative insensitivity to THP's modulation of these receptor subunits in Low LG offspring. These findings suggest that natural variations in maternal care influence anxiety-like and hedonic behavior through the modulation of the neurosteroid/GABAergic system.

The sexual preference of female rats is influenced by males' adolescent social stress history and social status.

Ongoing development of brain systems for social behaviour renders these systems susceptible to the influence of stressors in adolescence. We previously found that adult male rats that underwent social instability stress (SS) in mid-adolescence had decreased sexual performance compared with control males (CTL). Here, we test the hypotheses that SS in adolescence decreases the "attractiveness" of male rats as sexual partners compared with CTL rats and that dominance status is a protective factor against the effects of SS. The main prediction was that females would spend more time with CTL males than SS males, and that this bias would be greater for submissive than for dominant rats. Among dominant pairs (n=16), females preferred SS males, spending more time with and visiting more often SS than CTL males (each pair tested 5×), and SS males had shorter latencies to ejaculation, shorter inter-ejaculation intervals, and made more ejaculations compared with CTL males. Among submissive pairs (n=16), females spent more time with, visited more often, and displayed more paracopulatory behaviour with CTL than with SS males, and differences in sexual performance between SS and CTL males were modest and in the opposite direction from that in dominant pairs. The heightened motivation of SS males relative to CTL males for natural rewards may have attenuated differences in sexual performance in a paced mating context. In sum, the experience of stress in adolescence leads to long-lasting changes in males that are perceptible to females, are moderated by social status, and influence sexual behaviour.

Transgenerational Transmission of the Effect of Gestational Ethanol Exposure on Ethanol Use-Related Behavior.

BACKGROUND: Prenatal alcohol exposure (PAE) enhances the risk for alcoholism by increasing the propensity to consume alcohol and altering neurophysiological response to alcohol challenge. Trans-generationally transmittable genetic alterations have been implicated in these behavioral changes. To date, transgenerational transmission of PAE-induced behavioral responses to alcohol has never been experimentally investigated. Therefore, we explored the transgenerational transmission of PAE-induced behavioral effects across 3 generations. METHODS: Pregnant Sprague Dawley dams received 1 g/kg ethanol (EtOH) or water daily on gestational days 17 through 20 via gavage, or remained untreated in their home cages. To produce second filial (F2) or F3 generations, similarly treated adult F1 or F2 offspring were mated and left undisturbed through gestation. On postnatal day (PND) 14, male and female F1, F2, and F3 offspring were tested for consumption of 5% (w/v) EtOH (in water), or water. Using the loss of righting reflex (LORR) paradigm on PND 42, F1 and F2 adolescent male offspring were tested for sensitivity to acute EtOH-induced sedation-hypnosis at 3.5 or 4.5 g/kg dose. F3 male adolescents were similarly tested at 3.5 g/kg dose. Blood EtOH concentration (BEC) was measured at waking. RESULTS: EtOH exposure increased EtOH consumption compared to both water and untreated control groups in all generations. EtOH-treated group F1 and F2 adolescents displayed attenuated LORR duration compared to the water group. No attenuated LORR was observed in the F3 generation. BEC at waking corroborated with the significant LORR duration differences while also revealing differences between untreated control and water groups in F1 and F2 generations. CONCLUSIONS: Our results provide novel behavioral evidence attesting that late gestational moderate EtOH exposure increases EtOH intake across 3 generations and may alter sensitivity to EtOH-induced sedation-hypnosis across 2 generations.

Can low-level ethanol exposure during pregnancy influence maternal care? An investigation using two strains of rat across two generations.

Gestational alcohol use is well documented as detrimental to both maternal and fetal health, producing an increase in offspring's tendency for alcoholism, as well as in behavioral and neuropsychological disorders. In both rodents and in humans, parental care can influence the development of offspring physiology and behavior. Animal studies that have investigated gestational alcohol use on parental care and/or their interaction mostly employ heavy alcohol use and single strains. This study aimed at investigating the effects of low gestational ethanol dose on parental behavior and its transgenerational transmission, with comparison between two rat strains. Pregnant Sprague Dawley (SD) and Long Evans (LE) progenitor dams (F0) received 1g/kg ethanol or water through gestational days 17-20 via gavage, or remained untreated in their home cages. At maturity, F1 female offspring were mated with males of the same strain and treatment and were left undisturbed through gestation. Maternal behavior was scored in both generations during the first six postnatal days. Arch-back nursing (ABN) was categorized as: 1, when the dam demonstrated minimal kyphosis; 2, when the dam demonstrated moderate kyphosis; and 3, when the dam displayed maximal kyphosis. Overall, SD showed greater amounts of ABN than LE dams and spent more time in contact with their pups. In the F0 generation, water and ethanol gavage increased ABN1 and contact with pups in SD, behaviors which decreased in treated LE. For ABN2, ethanol-treated SD dams showed more ABN2 than water-treated dams, with no effect of treatment on LE animals. In the F1 generation, prenatal exposure affected retrieval. Transgenerational transmission of LG was observed only in the untreated LE group. Strain-specific differences in maternal behavior were also observed. This study provides evidence that gestational gavage can influence maternal behavior in a strain-specific manner. Our results also suggest that the experimental procedure during gestation and genetic variations between strains may play an important role in the behavioral effects of prenatal manipulations.

Estrogenic mediation of serotonergic and neurotrophic systems: implications for female mood disorders.

Clinical research has demonstrated a significant sex difference in the occurrence of depressive disorders. Beginning at pubertal onset, women report a higher incidence of depression than men. Women are also vulnerable to the development of depressive disorders such as premenstrual dysphoric disorder, postpartum depression, and perimenopausal depression. These disorders are associated with reproductive stages involving changes in gonadal hormone levels. Specifically, female depression and female affective behaviors are influenced by estradiol levels. This review argues two major mechanisms by which estrogens influence depression and depressive-like behavior: through interactions with neurotrophic factors and through an influence on the serotonergic system. In particular, estradiol increases brain derived neurotrophic factor (BDNF) levels within the brain, and alters serotonergic expression in a receptor subtype-specific manner. We will take a regional approach, examining these effects of estrogens in the major brain areas implicated in depression. Finally, we will discuss the gaps in our current knowledge of the effects of estrogens on female depression, and the potential utility for estrogen receptor modulators in treatment for this disorder.

Variations in maternal care associated with differences in female rat reproductive behavior in a group-mating environment.

Maternal care influences the development of sexual behavior in pair mating rats, under laboratory conditions. This study examined the effect of variations in maternal care in a group-mating condition. Groups of two low and two high licking/grooming (LG) female offspring mated with two males in a large pacing chamber for 36 hr. Sexual behaviors were scored for the first 15 vaginal-cervical stimulations (VCS) and the entire 36 hr. Low LG females spent more time mating, required more time to receive an intromission after entering the male compartment. They also received more ejaculations compared to high LG females during the first 15 VCS. This difference disappeared as mating continued. Males were more responsive to high than low females. No pregnancy rate difference was seen between the two female phenotypes, demonstrating that variation in maternal care received results in two mating strategies that are both reproductively successful under group-mating conditions.

Maternal care associates with play dominance rank among adult female rats.

Variations in maternal care influence important life history traits that determine reproductive fitness. The adult female offspring of mothers that show reduced levels of pup licking/grooming (LG; i.e., low-LG mothers) show increased defensive responses to stress, accelerated pubertal development, and greater sexual receptivity than the female offspring of high-LG mothers. Amongst several species an accelerated pattern of reproductive development is associated with increased dominance-related behaviors and higher social rank. We hypothesize that rats from low-LG dams may thus also secure higher social rank as a means to compete for limited resources with conspecifics. In this study, social interactions were observed in triads of adult female rats aged p90 that received low, mid, and high levels of pup LG over the first week of life. Low- and mid-LG females had the highest pinning scores and high-LG rats the lowest, showing that low- and mid-LG adult females engage in greater play dominance-related behavior. Likewise, low- and mid-LG rats spent significantly more time drinking following 24 hr of water deprivation in a water competition test thus allowing them to secure a limited resource more easily than high-LG rats. Interestingly, pinning by play dominant females was increased when subordinates were sexually receptive (proestrus/estrus), suggestive of a process of reproductive suppression. Some evidence suggests that low-LG and mid-LG rats also show greater fecundity than high-LG rats. Variations in maternal care may thus have a long-term influence on the development of play dominance and possibly social rank in the female rat, which might contribute to reproductive success within a competitive environment.

Deficits in male sexual behavior in adulthood after social instability stress in adolescence in rats.

There is increasing evidence that exposure to stressors in adolescence has long-lasting effects on emotional and cognitive behavior, but little is known as to whether reproductive functions are affected. We investigated appetitive and consummatory aspects of sexual behavior in male rats that were exposed to chronic social instability stress (SS, n=24) for 16 days in mid-adolescence compared to control rats (CTL, n=24). Over five sexual behavior test sessions with a receptive female, SS rats made fewer ejaculations (p=0.02) and had longer latencies to ejaculation (p=0.03). When only data from rats that ejaculated in the fifth session were analyzed, SS rats (n=18) had reduced copulatory efficiency (more mounts and intromissions before ejaculation) compared to CTL rats (n=19) (p=0.004), and CTL rats were twice as likely as SS rats to make more than one ejaculation in the fifth session (p=0.05). Further, more CTL (14/24) than SS (5/25) rats ejaculated in four or more sessions (p=0.05). SS rats had lower plasma testosterone concentrations than CTL rats (p=0.05), but did not differ in androgen receptor, estrogen receptor alpha, or Fos immunoreactive cell counts in the medial preoptic area. The groups did not differ in a partner preference test administered between the fourth and fifth sexual behavior session. The results suggest that developmental history contributes to individual differences in reproductive behavior, and that stress exposures in adolescence may be a factor in sexual sluggishness.

The role of oxytocin in mating and pregnancy.

The hormone oxytocin (OT) is released both centrally and peripherally during and after mating. Although research in humans suggests a central role in sexuality, the most reliable findings to date involve peripheral activation. This review will discuss these results and will particularly focus on understanding the most recent findings from fMRI data and the effects of exogenous peripheral OT administration. We will then consider hypotheses of the roles played by central and systemic OT release as well as their control and modulation in the female, summarizing recent findings from animal research. Finally, we will discuss the contribution of OT to the initiation of pregnancy in rodents. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.

Maternal programming of reproductive function and behavior in the female rat.

Parental investment can be used as a forecast for the environmental conditions in which offspring will develop to adulthood. In the rat, maternal behavior is transmitted to the next generation through epigenetic modifications such as methylation and histone acetylation, resulting in variations in estrogen receptor alpha expression. Natural variations in maternal care also influence the sexual strategy adult females will adopt later in life. Lower levels of maternal care are associated with early onset of puberty as well as increased motivation to mate and greater receptivity toward males during mating. Lower levels of maternal care are also correlated with greater activity of the hypothalamus-pituitary-gonadal axis, responsible for the expression of these behaviors. Contrary to the transition of maternal care, sexual behavior cannot simply be explained by maternal attention, since adoption studies changed the sexual phenotypes of offspring born to low caring mothers but not those from high caring dams. Indeed, mothers showing higher levels of licking/grooming have embryos that are exposed to high testosterone levels during development, and adoption studies suggest that this androgen exposure may protect their offspring from lower levels of maternal care. We propose that in the rat, maternal care and the in utero environment interact to influence the reproductive strategy female offspring display in adulthood and that this favors the species by allowing it to thrive under different environmental conditions.

Maternal influences on the sexual behavior and reproductive success of the female rat.

In many species, including humans, there is evidence for parental effects on within-sex variations in reproductive behavior. In the present studies we found that variations in postnatal maternal care were associated with individual differences in female sexual behavior in the rat. Females born to and reared by dams that showed enhanced pup licking/grooming (i.e., High LG mothers) over the first week postpartum showed significantly reduced sexual receptivity and alterations in the pacing of male mounting (i.e., longer inter-intromission intervals) observed in a paced mating test. There were minimal effects on the sexual behavior of the male offspring. The female offspring of High LG mothers showed a reduced lordosis rating, a decreased mount:intromission ratio, received fewer ejaculations and were less likely to achieve pregnancy following mating in the paced mating context. The data suggest maternal influences on the sexual development of the female rat that are functionally relevant for reproductive success. Together with previous studies these findings imply that maternal care can 'program' reproductive strategies in the female rat.

The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care.

There are profound maternal effects on individual differences in defensive responses and reproductive strategies in species ranging literally from plants to insects to birds. Maternal effects commonly reflect the quality of the environment and are most likely mediated by the quality of the maternal provision (egg, propagule, etc.), which in turn determines growth rates and adult phenotype. In this paper, we review data from the rat that suggest comparable forms of maternal effects on both defensive responses to threat and reproductive behavior and which are mediated by variations in maternal behavior. Ultimately, we will need to contend with the reality that neural development, function and health are defined by social and economic influences.

Medullary noradrenergic neurons release norepinephrine in the medial amygdala in females in response to mating stimulation sufficient for pseudopregnancy.

In the female rat, stimuli from the uterine cervix and vagina are carried to the brain areas involved in the mating-induced pseudopregnancy (PSP) response via the ventral noradrenergic bundle. Noradrenergic neurons projecting through this tract synapse in many forebrain areas including the amygdala, and neurons in the posterodorsal medial amygdala (MePD) are activated following mating. The goal of this experiment was to investigate whether norepinephrine (NE) is released into the MePD after mating using microdialysis and to determine the origin of this release. Ovariectomized estrogen- and progesterone-treated rats were implanted unilaterally with guide cannulae aimed at the MePD. Females were placed with males until they received 15 intromissions (15I), 5 intromissions (5I) or 15 mounts-without-intromission (MO). Dialysate samples collected every 20 min for 2 h before to 3 h after mating were analyzed for NE using HPLC with electrochemical detection. A significant increase in mean NE release in the MePD was seen at 80 min after mating onset in females receiving 15I, and no increase was seen in animals receiving 5I or MO. The time of peak NE release varied in 15I animals from 60 to 160 min after mating. Mean baseline levels of NE did not differ between groups. The retrograde tracer FluoroGold (FG), administered through the probe after cessation of dialysis sampling, was observed within identified noradrenergic cells primarily within the A1 and A2 cell groups. Infusion of anti-dopamine-beta-hydroxylase-saporin (DBH-SAP) into the MePD lesioned noradrenergic neurons located in the A1 and A2 cell groups. Because high levels of NE release occurred in the MePD only after the females received a number of intromissions sufficient to induce PSP, these results suggest that NE release within the MePD may be important for the establishment of PSP.

Co-regulation of female sexual behavior and pregnancy induction: an exploratory synthesis.

This paper will review both new and old data that address the question of whether brain mechanisms involved in reproductive function act in a coordinated way to control female sexual behavior and the induction of pregnancy/pseudopregnancy (P/PSP) by vaginocervical stimulation. Although it is clear that female sexual behavior, including pacing behavior, is important for induction of P/PSP, there has been no concerted effort to examine whether or how common mechanisms may control both functions. Because initiation of P/PSP requires that the female receive vaginocervical stimulation, central mechanisms controlling P/PSP may be modulated by or interactive with those that control female sexual behavior. This paper presents a synthesis of the literature and recent data from our lab for the purpose of examining whether there are interactions between behavioral and neuroendocrine mechanisms which reciprocally influence both reproductive functions.