Social cues elicit sexual behavior in subordinate Damaraland mole-rats independent of gonadal status.

Damaraland mole-rats (Fukomys damarensis) are among a small number of eusocial mammals. Eusociality is a social system where only a few individuals within a colony engage in direct reproduction, while remaining subordinate members are non-breeders and support reproductive efforts of breeding individuals. Inbreeding avoidance precludes mating between subordinate siblings and between offspring and parents. Interestingly, non-breeders readily attempt to mate with unrelated opposite-sex individuals. This is unusual since the non-breeding females do not attain puberty while in their natal colony. Based on this finding, the present study investigated the role of the gonads in the regulation of mating behaviors in this species and identified the mechanism of inbreeding avoidance. Gonadal-intact and gonadectomized non-breeders from different colonies were removed from their colonies and tested for the expression of sexual behavior. Results indicated that gonadal status had only minor effects on the expression of sexual behavior in either males or females. In a second experiment, sexual behaviors were absent between opposite-sex siblings so long as they had frequent contact with each other; however, following 5 weeks of separation, sexual behavior between these siblings was robustly expressed. Thus, Damaraland mole-rats avoid establishing mating relationships with familiar individuals but will readily mate with unfamiliar individuals of the opposite sex, with genetic relatedness apparently playing little role. The initiation of sexual behavior in Damaraland mole-rats does not require the presence of the gonads, but does require that the members of the pair have not been in contact with one another for at least several weeks.

Androgen receptor distribution in the social decision-making network of eusocial naked mole-rats.

Naked mole-rats are highly social rodents that live in large groups and exhibit a strict reproductive and social hierarchy. Only a few animals in each colony breed; the remainder are non-reproductive and are socially subordinate to breeders. We have examined androgen receptor immunoreactive (AR+) cells in brain regions comprising the recently described social decision-making network in subordinate and breeder naked mole-rats of both sexes. We find that subordinates have a significantly higher percentage of AR+ cells in all brain regions expressing this protein. By contrast, there were no significant effects of sex and no sex-by-status interactions on the percentage of AR+ cells. Taken together with previous findings, the present data complete a systematic assessment of the distribution of AR protein in the social decision-making network of the eusocial mammalian brain and demonstrate a significant role for social status in the regulation of this protein throughout many nodes of this network.

Neuroendocrinology and sexual differentiation in eusocial mammals.

Sexual differentiation of the mammalian nervous system has been studied intensively for over 25 years. Most of what we know, however, comes from work on relatively non-social species in which direct reproduction (i.e., production of offspring) is virtually the only route to reproductive success. In social species, an individual's inclusive fitness may include contributions to the gene pool that are achieved by supporting the reproductive efforts of close relatives; this feature is most evident in eusocial organisms. Here, we review what is known about neuroendocrine mechanisms, sexual differentiation, and effects of social status on the brain and spinal cord in two eusocial mammals: the naked mole-rat and Damaraland mole-rat. These small rodents exhibit the most rigidly organized reproductive hierarchy among mammals, with reproduction suppressed in a majority of individuals. Our findings suggest that eusociality may be associated with a relative lack of sex differences and a reduced influence of gonadal hormones on some functions to which these hormones are usually tightly linked. We also identify neural changes accompanying a change in social and reproductive status, and discuss the implications of our findings for understanding the evolution of sex differences and the neuroendocrinology of reproductive suppression.

Distribution of vasopressin in the brain of the eusocial naked mole-rat.

Naked mole-rats are eusocial rodents that live in large subterranean colonies in which one queen breeds with one to three males. All other animals are nonbreeding subordinates. The external features of male and female subordinates, including their genitalia, are remarkably monomorphic, as is their behavior. Because vasopressin (VP) is associated with social behaviors and sex differences in other species, its distribution in naked mole-rats was of interest. We used immunohistochemistry to examine VP in the brains of subordinate and breeding naked mole-rats of both sexes. As in other mammals, VP-immunoreactive (-ir) somata were found in the paraventricular (PVN) and supraoptic nuclei (SON) and VP-ir projections from these nuclei ran through the internal and external zone of the median eminence. However, naked mole-rats had very few VP-ir cells in the bed nucleus of the stria terminalis (BST) and none in the suprachiasmatic nucleus (SCN); the extensive network of fine-caliber VP-ir fibers usually seen in projection sites of the BST and SCN were also absent. Equally unexpected was the abundance of large-caliber VP-ir fibers in the dorsomedial septum. VP immunoreactivity was generally similar in all groups, with the exception of VP-ir cell number in the dorsomedial hypothalamus (DMH). Breeders had a population of labeled cells in the DMH that was absent, or nearly absent, in subordinates. Future studies on the function of VP in these areas are needed to determine how the atypical distribution of VP immunoreactivity relates to eusociality and the unusual physiology of naked mole-rats.

Influence of gonadal sex hormones on behavioral components of the reproductive hierarchy in naked mole-rats.

Naked mole-rats (Heterocephalus glaber) are fossorial, eusocial rodents that live in colonies which typically include 60-80 individuals. Generally, only one of the females and 1-3 of the males in a colony are reproductives. The reproductives engage in mutual genital nuzzling behavior that is rarely exhibited by subordinates (non-reproductives). Thus, genital nuzzling may represent a mechanism of bonding and/or specific recognition between reproductive individuals. We investigated whether gonadal hormones are involved in the maintenance of genital nuzzling behavior and mating behaviors in isolated pairs of mole-rats and also in established breeding pairs of mole-rats within colonies. We also explored whether sex hormone deprivation would alter the strict partner preference for performance of nuzzling within colonies. Our results indicate (a) considerable variation between pairs in the frequency of nuzzling, (b) a reduction in the frequency of nuzzling following castration of the male and restoration of the 'baseline' frequency after replacement of testosterone in castrated males, (c) the failure of either castration or combined castration and ovariectomy to eliminate genital nuzzling in established pairs, and (d) the exhibition of nuzzling behavior by some of the subordinates in all three experimental colonies beginning several weeks after gonadectomy of both of the reproductives. No cases of lordosis behavior were seen during the approximately 109 h of behavioral observations. This is not surprising, since female mole-rats have an approximately 30-day ovulatory cycle, and lordosis only occurs during a peri-ovulatory period of a few hours. A total of 44 cases of mounting behavior were recorded; all these involved breeding males in colonies or males from isolated pairs, and all occurred when males were either gonad-intact or castrated with testosterone replacement. Thus, in contrast to nuzzling behavior, male sex behavior appeared to be eliminated during androgen deprivation.

Early photoperiod history and short-day responsiveness in Siberian hamsters.

Siberian hamsters exhibit seasonal, photoperiod influenced cycles of reproductive activity, body size, pelage characteristics, and thermoregulatory behavior. Laboratory populations generally exhibit inter-individual variability in expression of photoperiod responsiveness, with a subset of individuals that fail to show the species typical responses to short photoperiod. This variability is partly explained by a genetic component, as it has been possible to increase the number of short-day nonresponders by artificial selection. Responsiveness to short photoperiod is also substantially influenced by photoperiod history in this species; hamsters that have been raised under long (16L) or very long (18L) day lengths are less likely to exhibit winter-type responses to short days as compared to hamsters raised under an intermediate (14L) day length. In the present experiment, we examined effects of age and early photoperiod history in a strain of Siberian hamsters that had been selected for short-day nonresponsiveness. Hamsters transferred into short photoperiod on the day of birth were uniform in exhibiting winter-type responses. However, hamsters raised until 25 days of age in either continuous illumination or in 16L exhibited variation in responsiveness when subsequently moved into short photoperiod. We conclude that virtually all hamsters of the short-day nonresponsive strain are born responsive to short days. Subsequent development of resistance to potential short day effects is dependent on age and/or photoperiod history.