The ownership signature in mouse scent marks is involatile.

Male house mice advertise their territory ownership through urinary scent marks and use individual-specific patterns of major urinary proteins (MUPs) to discriminate between their own scent and that of other males. It is not clear whether recognition occurs through discrimination of the non-volatile proteins or protein-ligand complexes (direct model), or by the detection of volatile ligands that are released from MUPs (indirect model). To examine the mechanism underlying individual scent mark signatures, we compared investigatory and countermarking responses of male laboratory mice presented with male scent marks from a strain with a different MUP pattern, when they could contact the scent or when contact was prevented by a porous nitrocellulose sheet to which proteins bind. Mice investigated scent marks from other males whether these were covered or not, and biochemical analysis confirmed that the porous cover did not prevent the release of volatiles from scent marks. Having gained information through investigation, mice increased their own scent marking only if they had direct contact with another male's urine, failing to do this when contact was prevented. Individual signatures in scent marks thus appear to be carried by non-volatile proteins or by non-volatile protein-ligand complexes, rather than by volatiles emanating from the scent.

Individual recognition in mice mediated by major urinary proteins.

The ability to recognize individuals is essential to many aspects of social behaviour, such as the maintenance of stable social groups, parent-offspring or mate recognition, inbreeding avoidance and the modulation of competitive relationships. Odours are a primary mediator of individuality signals among many mammals. One source of odour complexity in rodents, and possibly in humans, resides in the highly polymorphic major histocompatibility complex (MHC). The olfactory acuity of mice and rats allows them to distinguish between the urinary odours of congenic strains differing only in single genes within the MHC, although the chemical mediators or odorants are unknown. However, rodent urine also contains a class of proteins, termed major urinary proteins (MUPs), that bind and release small volatile pheromones. We have shown that the combinatorial diversity of expression of MUPs among wild mice might be as great as for MHC, and at protein concentrations a million times higher. Here we show in wild house mice (Mus domesticus) that urinary MUPs play an important role in the individual recognition mechanism.

The consequences of inbreeding for recognizing competitors.

Extreme inbreeding will compromise an animal's ability to discriminate between individuals and, thus, assess familiarity and kinship with conspecifics. In rodents, a large component of individual recognition is mediated through chemical communication. The counter-marking of competitor males' scent marks provides a measure of discrimination between their own scent and that from other individuals. We investigated whether males in common outbred (ICR(CD-1) and TO) and inbred (BALB/c) strains of laboratory mice could recognize the urinary scents of other individuals by measuring their investigation and counter-marking responses. Dominant males of outbred strains investigated and counter-marked scents from other males, whether of the same or another strain. Dominant inbred BALB/c males investigated but did not counter-mark their own strain scents, counter-marking only those from another strain. They did not use environmentally induced status differences in odours to recognize scents from other males. The inability of the inbred mice to discriminate between their own scent marks and those of other males is likely to alter their competitive behaviour, which could influence responses in experiments and the welfare of caged laboratory mice.

Manipulation of postnatal testosterone levels affects phallic and clitoral development in infant rhesus monkeys.

Male primates exhibit marked elevation of circulating testosterone levels during the early postnatal period. The aim of this project was to test whether experimental manipulation of circulating testosterone levels in male and female infant rhesus monkeys affected development of the external genitalia during the first six months of life. Four groups of infants were studied. Seven control male infants exhibited high circulating testosterone levels during the first three months of life. Seven males were treated with a GnRH agonist (avorelin) from the first week of life onwards, which suppressed the postnatal testosterone surge. Ten control females exhibited low circulating testosterone levels during the early postnatal period. Administration of testosterone to 10 females resulted in high circulating levels in these infants. Fortnightly blood samples and genital measurements were taken from all infants during the first six months of life. Growth of the penis of avorelin-treated males was significantly retarded when compared to control males. Average length of the penis at six months of age was significantly (p = 0.012) smaller for avorelin-treated males (25.2 +/- 2.8 mm) than for control males (37.3 +/- 3.0 mm). Avorelin-treated males attained only around 50% detachment of the prepuce from the glans of the penis, while control males averaged 90% detachment. Treatment of females with testosterone resulted in significant growth of the clitoris in comparison to control females. The growth rates of the penis of control males and clitorides of testosterone-treated females were similar and greatest during the first two months of life. Gain in body weight was not affected by either hormonal manipulation. It is concluded that manipulation of circulating testosterone levels during the early postnatal period affects penile and clitoral development of infant rhesus monkeys. This postnatal period may therefore represent an important stage in penile development in primates.

Why do male ICR(CD-1) mice perform bar-related (stereotypic) behaviour?

Prolonged interaction with cage bars by captive mammals (usually classed as stereotypic) may reflect poor welfare. Such behaviour may arise from motivation to investigate the external environment or to escape captivity. However, these hypotheses have not been explicitly tested. We raised mice, Mus musculus, to adulthood in modified laboratory cages with two sets of bars at the top and side of the cage. One set provided a potential escape route, and half of each set was backed by Perspex to reduce cues from the external environment. We predicted where mice should interact with the bars according to their motivational priorities. Body weights were recorded weekly to study the relationship between physical development and bar-related behaviour. Serum corticosterone was measured to monitor the effect of bar-related behaviour on stress physiology. Mice preferred to interact with bars where external cues were detectable. As adults, mice responded more to the bars providing a potential exit, though this was affected by the exit location. Corticosterone titres were higher in mice whose potential exit was situated at the cage top. Response to the bars was apparently restricted by the physical development of mice, particularly among those whose potential exit was situated in the cage top.

The socioendocrinology of adolescent development in male rhesus monkeys (Macaca mulatta).

Observations were made on four captive breeding groups of rhesus monkeys in order to measure hormonal, behavioral, and genital changes in adolescent males during the annual mating season. Three questions were addressed with regard to possible effects of social environment upon reproductive maturation: (1) Does male agonistic rank influence adolescent development? (2) Does affiliation between adolescent males and adult females during the mating season influence the males' reproductive development? (3) Does maternal rank exert any effect upon reproductive maturation in adolescent sons? In many (but not all) cases male rank was positively correlated with circulating testosterone and testes weights during the mating season. Affiliative behavior (allogrooming and sexual interactions) between adolescents and adult females in their social groups bore no relationship to the degree of reproductive maturation in males. Mounts involving intromission were infrequent, but sons of high-ranking mothers gained significantly more intromissions than sons of lower-ranking females. Maternal rank was also found to correlate with circulating testosterone levels, testes weights, growth of the baculum (os penis), and maintenance of body weight in adolescent sons during the mating season. By contrast, levels of beta-endorphin in the cerebrospinal fluid of adolescent males did not correlate with social rank, testosterone levels, or genital development. These findings point to possible effects of maternal rank, as well as intermale agonistic rank, in determining reproductive maturation during adolescence in the male rhesus monkey.

Effects of altering testosterone in early infancy on social behaviour in captive yearling rhesus monkeys.

Thirteen male and twenty female rhesus monkeys (Macaca mulatta), aged 9-12 months, living as members of long term captive social groups, were observed in order to quantify sex differences in a variety of behaviour patterns. Six males had been treated with a GnRH agonist (Meterelin: M) during their first six postnatal months, in order to block the surge of testosterone which occurs at this time. Ten females had been treated with testosterone (T) during their first six months, in order to mimic the postnatal T surge seen in males. The remaining 7 males and 10 females acted as control subjects. Marked sex differences were measured in frequencies of play and socio-sexual behaviour in these juvenile monkeys. However, neither M nor T treatments produced any significant changes in frequencies of these behaviour patterns. Although M-treated males showed a tendency (p < 0.1) to groom others for longer periods than control males, and control females tended to spend more time alone than T-treated females, we were unable to measure any significant (p < 0.05) effects of either M- or T-treatment upon affiliative behaviour in juvenile rhesus monkeys. We conclude, therefore, that the postnatal T surge in male rhesus monkeys does not affect development of sexually dimorphic and associated patterns of behaviour. Presumably, organisational effects of T upon these behaviour patterns must be completed before birth in this species.

Primate brain evolution: genetic and functional considerations.

Functionally distinct regions of the brain to which maternal and paternal genomes contribute differentially (through genomic imprinting) have developed differentially over phylogenetic time. While certain regions of the primate forebrain (neocortex, striatum) have expanded relative to the rest of the brain, other forebrain regions have contracted in size (hypothalamus, septum). Areas of relative expansion are those to which the maternal genome makes a substantial developmental contribution. This may be significant with respect to the importance of primate forebrain expansion in the development of complex behavioural strategies and the way in which these are deployed, especially by the matriline. In many primate societies the maintenance of social cohesion and group continuity over successive generations is dependent on the matriline, with high ranking females producing high ranking daughters that stay within the group. Regions of relative contraction are those to which the paternal genome makes a differential contribution and these are target areas for gonadal hormones, which is congruent with the diminished role for gonadal hormones in the emancipation of primate reproductive behaviour.

Birth sex ratios and maternal social rank in a captive colony of rhesus monkeys (Macaca mulatta).

Data from a 35-year study of rhesus macaques (Macaca mulatta) at Madingley, Cambridge, were used to investigate sex ratio biases associated with maternal rank. Data were available from two colonies, the Old colony (1960-81) and New colony (1982-93). Overall, top-ranking mothers gave birth to 30.9% sons, while non-top mothers gave birth to 58.4% sons. Among non-top mothers, middle- and bottom-ranking ones had 59.0 and 55.0% sons, respectively. Top mothers' daughter biases were strongest in matrilines with two adult females in the year the infants were conceived (15.4 sons and 14.3% sons in Old and New colonies). Non-top mothers' son biases (88.9 and 71.0% in Old and New colonies) were strongest in matrilines with 3 females. The findings are discussed in relation to the colonies' small matriline sizes and data on breeding performance and infant survival, which indicate the costs to mothers of different rank of having different sex infants. Overall, top-ranking mothers were more likely to breed in two successive years (78.6%) than non-top mothers (56.7%). Infant survival to 7 days was significantly higher in the New colony (89.0%) than the Old colony (75.3%), with daughters born to Old colony mothers doing especially poorly. We point out that between-group and between-species comparisons of sex ratio effects depend critically on how females are assigned to rank categories, and require information about divergences of sex ratios from 50:50 in each category. © 1996 Wiley-Liss, Inc.

Effects of opioid receptor blockade on the social behavior of rhesus monkeys living in large family groups.

Rhesus monkeys of 9 weeks, 48 weeks, 100 weeks, 150 weeks of age (young subjects), or mature parous females that were not lactating were given acute single doses of the opioid antagonist naloxone (0.5 mg/kg) and vehicle on different days and observed in their familial social groups. Naloxone increased the occurrence of affiliative behaviours. Young subjects spent more time in contact with their mothers but showed no changes in social grooming. Maternal contact was actively sought through contact vocalizations, decreasing proximity, and, for the youngest infants, increased attempts to suckle. Mature females made more solicitations for grooming and received more grooming from their companions. These results are interpreted in terms of naloxone blocking the positive effect arising from social contact and thus causing subjects to seek further affiliative comfort.

Opioid receptor blockade reduces maternal affect and social grooming in rhesus monkeys.

Seven lactating female rhesus macaques, housed in social groups, were administered with low doses (0.5 mg/kg) of the opioid antagonist naloxone when their infants were 4, 6, 8, and 10 weeks old. A control group received saline. Mothers receiving naloxone were involved in less grooming with other group members, and were less protective towards their infants. By infant-age week 8 they also groomed their infants less, while other monkeys groomed the infants more. Other behavioural measures of mother-infant interactions were not altered. With time, from infant-age week 6 onwards, some short-lived dysphoric conditioned drug responses to naloxone became apparent, although these were not correlated with the decline in social interaction. These results are interpreted in terms of possible interference of naloxone with maternal affect.

Anxiety in rhesus monkey infants in relation to interactions with their mother and other social companions.

In this study the anxiety-related components of rhesus monkey infant behavior at an early stage of social development were examined. Eight rhesus infants (age 30-40 weeks) belonging to 3 captive groups were administered with an anxiogenic drug (beta-CCE; 0.2 mg/kg) and an anxiolytic drug (midazolam; 0.2 mg/kg). Saline solution was used as placebo. All infants were tested twice with each drug (four times with placebo) and their behavioral interactions with their mother and other social companions were recorded in 1-hr observation sessions. No convulsant or sedative effects of the drugs were observed. beta-CCE was associated with an increase in time spent by the infant with its mother and a concomitant reduction in proximity with other individuals and in social play. Midazolam did not affect the mother-infant interaction but increased the infant's locomotor activity away from the mother and its proximity and social play with juveniles and subadults when compared to peers. These results suggest that, although infant anxiety can be experimentally induced, it is not a major component of the mother-infant relationship. Infant anxiety, however, might affect the formation of other social bonds and play a part in the development of avoidance responses toward other individuals.