Bernard Wallner

The evolution of violence in men: the function of central cholesterol and serotonin.

Numerous studies point to central serotonin as an important modulator of maladaptive behaviors. In men, for instance, low concentrations of this neurotransmitter are related to hostile aggression. A key player in serotonin metabolism seems to be central cholesterol. It plays a fundamental role in maintaining the soundness of neuron membranes, especially in the exocytosis transport of serotonin vesicles into the synaptic cleft. In this review, we attempt an evolutionary approach to the neurobiological basis of human male violence. Hominid evolution was shaped by periods of starvation but also by energy demands of an increasingly complex brain. A lack of food resources reduces uptake of glucose and results in a decreased energy-supply for autonomous brain cholesterol synthesis. Consequently, concentrations of neuromembrane cholesterol decrease, which lead to a failure of the presynaptic re-uptake mechanism of serotonin and ultimately to low central serotonin. We propose that starvation might have affected the larger male brains earlier than those of females. Furthermore, this neurophysiological process diminished the threshold for hostile aggression, which in effect represented a prerequisite for being a successful hunter or scavenger. In a Darwinian sense, the odds to acquire reliable energetic resources made those males to attractive spouses in terms of paternal care and mate support. To underpin these mechanisms, a hypothetical four-stage model of synaptic membrane destabilization effected by a prolonged shortage of high-energy, cholesterol-containing food is illustrated.

Second-to-fourth digit ratio and facial shape in boys: the lower the digit ratio, the more robust the face

During human ontogeny, testosterone has powerful organizational and activational effects on the male organism. This has led to the hypothesis that the prenatal environment (as studied through the second-to-fourth digit ratio, 2D : 4D) is not only associated with robust adult male faces that are perceived as dominant and masculine, but also that there is an activational step during puberty. To test the latter, we collected digit ratios and frontal photographs of right-handed Caucasian boys (aged 4–11 years) along with age, body height and body weight. Using geometric morphometrics, we show a significant relationship between facial shape and 2D : 4D before the onset of puberty (explaining 14.5% of shape variation; p = 0.014 after 10 000 permutations, n = 17). Regression analyses depict the same shape patterns as in adults, namely that the lower the 2D : 4D, the smaller and shorter the forehead, the thicker the eyebrows, the wider and shorter the nose, and the larger the lower face. Our findings add to previous evidence that certain adult male facial characteristics that elicit attributions of masculinity and dominance are determined very early in ontogeny. This has implications for future studies in various fields ranging from social perception to life-history strategies.

Social stimuli cause changes of plasma oxytocin and behavior in guinea pigs

The neuropeptide oxytocin (OXT) is a key factor in the initiation and regulation of sociosexual behavior. The present study analyzes the effects of cohabitation and social challenge on plasma OXT concentration rates in guinea pig pairs in relation to male sociosexual behavior. The cohabitation phase lasted 3 days. On day 4, the pair was socially challenged by introducing an unfamiliar male. Displayed male sexual behavior varied significantly during cohabitation, with peaks on day 1. Sociopositive behavior, i.e., side-by-side contact, was increased on days 3 and 4. Cohabitation per se led to elevated plasma OXT concentrations only in males. In contrast, both sexes reacted with increased plasma OXT concentrations to the social challenge (day 4). At that time, male OXT was significantly correlated with sexual behavior and female OXT with sociosexual behavior received from the partner. Additionally, pairs were synchronized in their OXT release during days 3 and 4. We conclude that cohabitation causes sexually dimorphic plasma OXT concentration patterns in guinea pigs. Secondly, the conformity of OXT release in both sexes may represent an endocrine marker for long-term cohabitation, which is reflected behaviorally by increased spatial proximity.

Whom to groom and for what? Patterns of grooming in female Barbary macaques (Macaca sylvanus).

Grooming is one of the most conspicuous social interactions among nonhuman primates. The selection of grooming partners can provide important clues about factors relevant for the distribution of grooming within a social group. We analyzed grooming behavior among 17 semi-free ranging female Barbary macaques (Macaca sylvanus). We tested whether grooming is related to kinship, rank and friendship. Furthermore, we tested whether grooming is reciprocated or exchanged for rank related benefits (i.e. lower aggression and increased tolerance whilst feeding). We found that in general grooming was reciprocally exchanged, directed up the hierarchy and at the same time affected by friendship and kinship. Grooming was more frequent among individuals with higher friendship values as well as amongst related individuals. We also divided our data set on the basis of rank difference and tested if different power asymmetries between individuals affected the tendency to exchange grooming for rank related benefits and grooming reciprocation. In support of our initial hypothesis our results show that the reciprocation of grooming was a significant predictor of grooming interactions between individuals of similar rank, but not between those individuals more distantly separated in the social hierarchy. However, we did not find any evidence for grooming being exchanged for rank related benefits in either data set. Our results, together with previously published studies, illustrate the behavioral flexibility of macaques. It is clear that multiple studies of the same species are necessary to gather the data required for the solid comparative studies needed to shed light on patterns of grooming behavior in primates.

Signatures of positive selection in the cis-regulatory sequences of the human oxytocin receptor (OXTR) and arginine vasopressin receptor 1a (AVPR1A) genes

BackgroundThe evolutionary highly conserved neurohypophyseal hormones oxytocin and arginine vasopressin play key roles in regulating social cognition and behaviours. The effects of these two peptides are meditated by their specific receptors, which are encoded by the oxytocin receptor (OXTR) and arginine vasopressin receptor 1a genes (AVPR1A), respectively. In several species, polymorphisms in these genes have been linked to various behavioural traits. Little, however, is known about whether positive selection acts on sequence variants in genes influencing variation in human behaviours.ResultsWe identified, in both neuroreceptor genes, signatures of balancing selection in the cis-regulative acting sequences such as transcription factor binding and enhancer sequences, as well as in a transcriptional repressor sequence motif. Additionally, in the intron 3 of the OXTR gene, the SNP rs59190448 appears to be under positive directional selection. For rs59190448, only one phenotypical association is known so far, but it is in high LD’ (>0.8) with loci of known association; i.e., variants associated with key pro-social behaviours and mental disorders in humans.ConclusionsOnly for one SNP on the OXTR gene (rs59190448) was a sign of positive directional selection detected with all three methods of selection detection. For rs59190448, however, only one phenotypical association is known, but rs59190448 is in high LD’ (>0.8), with variants associated with important pro-social behaviours and mental disorders in humans. We also detected various signatures of balancing selection on both neuroreceptor genes.

Impact of social environment on female chimpanzee reproductive cycles

The socio-sexual environment of a female is known to affect ovarian function. Increased male contact can enhance menstrual cycle regularity. Conversely, social deprivation constitutes a form of stress that often alters cyclicity and the secretion of reproductive hormones. The present study was carried out on captive female chimpanzees to examine possible interactions among housing conditions, menstrual cycle length, morphological changes in secondary sexual character expression and endocrine release patterns related to follicular and luteal function. Animals were housed over a period of 2 years either with a male conspecific or singly. Blood samples were collected over three cycles, and anogenital swelling changes registered to define menstrual cycle phases. Fecal sampling techniques were used to monitor cortisol as a measure of stress-load. Male presence seemed to affect female cyclicity. Females housed with a male had shorter and more regular cycles than singly housed females. Prolactin, gonadotropins and estradiol levels were generally higher in paired females during specific cycle phases. Group variation was not always significant. No differences were found in progesterone. Sexually cohabited females tended to have lower fecal cortisol metabolites immediately before and after maximum tumescence. We suggest that the close behavioral, physical and olfactory contact with a male conspecific can act as a sort of zeitgeber to modulate ovarian function by stabilizing the female cycle and, perhaps, enhancing folliculogenesis and ovulation.

Spatial learning and memory differs between single and cohabitated guinea pigs.

In socially-living animals, social enrichment enhances spatial learning and memory while separation from conspecifics can severely impair these abilities. In the present work, guinea pigs were kept in isolation or cohabitated in heterosexual pairs and then subjected to a labyrinth task. Latency-time to bait, error-rate, amount of movement and pre- and post-experimental cortisol (CORT) were registered. During a 5d-acquisition phase, single animals (N=19) showed a more efficient encoding of spatial information, with significantly decreased latency-time and error-rate over the time course. In contrast, cohabitated animals (N=19) did not show a significant improvement. Three days after acquisition, memory was tested in a retention test, under the same conditions. With regard to behavioral performance, there was no significant difference between cohabitated and single animals. Pre-experimental CORT was significantly higher in cohabitated animals when compared to single ones. Post-experimentally, CORT increased significantly in singles but not in cohabitated animals when compared to pre-experimental values. Thus, both groups did not differ from each other at that point. Social condition seemed to be an important modulator, in that learning and memory were more impaired in paired animals than in single ones. The failure of cohabitated animals to encode spatial memory more quickly may have been caused by a more chronically up-regulated HPA-axis. The post-experimental CORT increase of singles may be due to more efficient handling of short-term stress exposure.

Sex-Specific Effects of Diets High in Unsaturated Fatty Acids on Spatial Learning and Memory in Guinea Pigs

Unsaturated fatty acids (UFAs), including omega-3, omega-6 polyunsaturated and omega-9 monounsaturated fatty acids, are essential components and modulators of neuromembranes and may affect various aspects of physiology and cognition. UFAs are suggested to positively affect spatial learning and memory and also to diminish the negative consequences of physiological stress on cognitive abilities. Due to pronounced sex differences in neurophysiological functions, we hypothesize that these UFA-related effects might differ between male and female individuals. We therefore determined the effects of dietary UFAs on cognitive performances in a radial-Y-maze in male and female guinea pigs in relation to saliva cortisol concentrations, a marker for physiological stress. Animals were assigned to four treatment groups and maintained on diets enriched in either chia seeds (omega-3), walnuts (omega-6), or peanuts (omega-9), or a control diet. Female learning abilities throughout a three-day learning phase were positively affected by omega-3 and omega-9, as determined by a decreasing latency to pass the test and the number of conducted errors, while males generally showed distinct learning abilities, irrespective of the diet. A sex difference in learning performances was found in the control group, with males outperforming females, which was not detected in the UFA-supplemented groups. This was paralleled by significantly increased saliva cortisol concentrations in males throughout the cognition test compared to females. Three days after this learning phase, UFA-supplemented males and all females showed unchanged performances, while control males showed an increased latency and therefore an impaired performance. These results were corroborated by pronounced differences in the plasma UFA-status, corresponding to the different dietary treatments. Our findings indicate sex-specific effects of dietary UFAs, apparently enhancing spatial learning abilities only in females and protecting males from long-term memory impairment, while male learning abilities seem to be more strongly affected by an acute physiological stress response to the maze task.

Ownership of Dwelling Affects the Sex Ratio at Birth in Uganda

Background Socio-economic conditions can affect the secondary sex ratio in humans. Mothers under good environmental conditions are predicted to increase the birth rates of sons according to the Trivers-Willard hypothesis (TWH). This study analyzed the effects of ownership and non-ownership of dwellings on the sex ratio at birth (SRB) on a Ugandan sample. Methodology/Principal Findings Our investigation included 438,640 mothers aged between 12 and 54 years. The overall average SRB was 0.5008. Mothers who live in owned dwellings gave increased births to sons (0.5019) compared to those who live in non-owned dwellings (0.458). Multivariate statistics revealed the strongest effects of dwelling ownership when controlling for demographic and social variables such as marital status, type of marriage, mothers’ age, mothers’ education, parity and others. Conclusions/Significance The results are discussed in the framework of recent plausible models dealing with the adjustment of the sex ratio. We conclude that the aspect of dwelling status could represent an important socio-economic parameter in relation to SRB variations in humans if further studies are able to analyze it between different countries in a comparative way.

Non-invasive cortisol measurements as indicators of physiological stress responses in guinea pigs

Non-invasive measurements of glucocorticoid (GC) concentrations, including cortisol and corticosterone, serve as reliable indicators of adrenocortical activities and physiological stress loads in a variety of species. As an alternative to invasive analyses based on plasma, GC concentrations in saliva still represent single-point-of-time measurements, suitable for studying short-term or acute stress responses, whereas fecal GC metabolites (FGMs) reflect overall stress loads and stress responses after a species-specific time frame in the long-term. In our study species, the domestic guinea pig, GC measurements are commonly used to indicate stress responses to different environmental conditions, but the biological relevance of non-invasive measurements is widely unknown. We therefore established an experimental protocol based on the animals’ natural stress responses to different environmental conditions and compared GC levels in plasma, saliva, and fecal samples during non-stressful social isolations and stressful two-hour social confrontations with unfamiliar individuals. Plasma and saliva cortisol concentrations were significantly increased directly after the social confrontations, and plasma and saliva cortisol levels were strongly correlated. This demonstrates a high biological relevance of GC measurements in saliva. FGM levels measured 20 h afterwards, representing the reported mean gut passage time based on physiological validations, revealed that the overall stress load was not affected by the confrontations, but also no relations to plasma cortisol levels were detected. We therefore measured FGMs in two-hour intervals for 24 h after another social confrontation and detected significantly increased levels after four to twelve hours, reaching peak concentrations already after six hours. Our findings confirm that non-invasive GC measurements in guinea pigs are highly biologically relevant in indicating physiological stress responses compared to circulating levels in plasma in the short- and long-term. Our approach also underlines the importance of detailed investigations on how to use and interpret non-invasive measurements, including the determination of appropriate time points for sample collections.