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1.  Social Status and Sex Effects on Neural Morphology in Damaraland Mole-Rats, Fukomys damarensis 
Brain, Behavior and Evolution  2011;77(4):291-298.
We previously reported that in a eusocial rodent, the naked mole-rat (Heterocephalus glaber), traditional neural sex differences were absent; instead, neural dimorphisms were associated with breeding status. Here we examined the same neural regions previously studied in naked mole-rats in a second eusocial species, the Damaraland mole-rat (Fukomys damarensis). Damaraland mole-rats live in social groups with breeding restricted to a small number of animals. However, colony sizes are much smaller in Damaraland mole-rats than in naked mole-rats and there is consequently less reproductive skew. In this sense, Damaraland mole-rats may be considered intermediate in social organization between naked mole-rats and more traditional laboratory rodents. We report that, as in naked mole-rats, breeding Damaraland mole-rats have larger volumes of the principal nucleus of the bed nucleus of the stria terminalis and paraventricular nucleus of the hypothalamus than do subordinates, with no effect of sex on these measures. Thus, these structures may play special roles in breeders of eusocial species. However, in contrast to what was seen in naked mole-rats, we also found sex differences in Damaraland mole-rats: volume of the medial amygdala and motoneuron number in Onuf's nucleus were both greater in males than in females, with no significant effect of breeding status. Thus, both sex and breeding status influence neural morphology in Damaraland mole-rats. These findings are in accord with the observed sex differences in body weight and genitalia in Damaraland but not naked mole-rats. We hypothesize that the increased sexual dimorphism in Damaraland mole-rats relative to naked mole-rats is related to reduced reproductive skew.
doi:10.1159/000328640
PMCID: PMC3182041  PMID: 21701152
Bed nucleus of the stria terminalis; Damaraland mole-rat; Medial amygdala; Naked mole-rat; Onuf's nucleus; Paraventricular nucleus; Sex difference; Social status
2.  Social and Hormonal Triggers of Neural Plasticity in Naked Mole-Rats 
Behavioural brain research  2010;218(1):234-239.
Naked mole-rats are eusocial rodents that live in large social groups with a strict reproductive hierarchy. In each colony only a few individuals breed; all others are non-reproductive subordinates. We previously showed that breeders have increased volume of several brain regions linked to reproduction: the paraventricular nucleus of the hypothalamus (PVN), the principal nucleus of the bed nucleus of the stria terminalis (BSTp), and the medial amygdala (MeA). Breeders also have more large motoneurons in Onuf’s nucleus (ON) in the spinal cord, a cell group innervating perineal muscles that attach to the genitalia. Here, we sought to determine triggers for the neural changes seen in breeders. Specifically, we compared four groups of animals: subordinates, paired animals that did not reproduce, gonadally intact breeders, and gonadectomized breeders. We find that pairing alone is sufficient to cause breeder-like changes in volume of the PVN and cell size distribution in ON. In contrast, increases in BSTp volume were seen only in animals that actually reproduced. Those changes that were seen in successful breeders appear to be independent of gonadal steroids because long-term gonadectomy did not reverse the breeder-like neural changes in the PVN, BSTp or ON, although a trend for gonadectomized animals having larger MeA volumes was detected. Thus, neural changes associated with breeding status in naked mole-rats may be triggered by different aspects of the social and reproductive environment; once changes occur they are largely independent of gonadal hormones and may be permanent.
doi:10.1016/j.bbr.2010.11.056
PMCID: PMC3022096  PMID: 21130812
bed nucleus of the stria terminalis; naked mole-rat; neuroplasticity; Onuf’s nucleus; paraventricular nucleus; social status
3.  Neuroendocrinology and Sexual Differentiation in Eusocial Mammals 
Frontiers in neuroendocrinology  2009;30(4):519-533.
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.
doi:10.1016/j.yfrne.2009.04.010
PMCID: PMC2748139  PMID: 19416733
naked mole-rat; Damaraland mole-rat; sex difference; social status; reproductive hierarchy; eusociality; social system
4.  Social Structure Predicts Genital Morphology in African Mole-Rats 
PLoS ONE  2009;4(10):e7477.
Background
African mole-rats (Bathyergidae, Rodentia) exhibit a wide range of social structures, from solitary to eusocial. We previously found a lack of sex differences in the external genitalia and morphology of the perineal muscles associated with the phallus in the eusocial naked mole-rat. This was quite surprising, as the external genitalia and perineal muscles are sexually dimorphic in all other mammals examined. We hypothesized that the lack of sex differences in naked mole-rats might be related to their unusual social structure.
Methodology/Principal Findings
We compared the genitalia and perineal muscles in three African mole-rat species: the naked mole-rat, the solitary silvery mole-rat, and the Damaraland mole-rat, a species considered to be eusocial, but with less reproductive skew than naked mole-rats. Our findings support a relationship between social structure, mating system, and sexual differentiation. Naked mole-rats lack sex differences in genitalia and perineal morphology, silvery mole-rats exhibit sex differences, and Damaraland mole-rats are intermediate.
Conclusions/Significance
The lack of sex differences in naked mole-rats is not an attribute of all African mole-rats, but appears to have evolved in relation to their unusual social structure and reproductive biology.
doi:10.1371/journal.pone.0007477
PMCID: PMC2759003  PMID: 19829697
5.  DISTRIBUTION OF OXYTOCIN IN THE BRAIN OF A EUSOCIAL RODENT 
Neuroscience  2008;155(3):809-817.
Naked mole-rats are highly social rodents that live in large colonies characterized by a rigid social and reproductive hierarchy. Only one female, the queen, breeds. Most colony members are non-reproductive subordinates that work cooperatively to rear the young and maintain an underground burrow system. Little is known about the neurobiological basis of the complex sociality exhibited by this species. The neuropeptide oxytocin (Oxt) modulates social bonding and other social behaviors in many vertebrates. Here we examined the distribution of Oxt immunoreactivity in the brains of male and female naked mole-rats. As in other species, the majority of Oxt-immunoreactive (Oxt-ir) cells were found in the paraventricular and supraoptic nuclei, with additional labeled cells scattered throughout the preoptic and anterior hypothalamic areas. Oxt-ir fibers were found traveling toward and through the median eminence, as well as in the tenia tecta, septum, and nucleus of diagonal band of Broca. A moderate network of fibers covered the bed nucleus of the stria terminalis and preoptic area, and a particularly dense fiber innervation of the nucleus accumbens and substantia innominata was observed. In the brainstem, Oxt-ir fibers were found in the periaqueductal grey, locus coeruleus, parabrachial nucleus, nucleus of the solitary tract, and nuclueus ambiguus. The high levels of Oxt immunoreactivity in the nucleus accumbens and preoptic area are intriguing, given the link in other rodents between Oxt signaling in these regions and maternal behavior. Although only the queen gives birth or nurses pups in a naked mole-rat colony, most individuals actively participate in pup care.
doi:10.1016/j.neuroscience.2008.05.039
PMCID: PMC2614305  PMID: 18582538
sex differences; social hierarchy; naked mole-rat; Heterocephalus glaber; sociality; vasopressin
6.  SOCIAL STATUS AND SEX INDEPENDENTLY INFLUENCE ANDROGEN RECEPTOR EXPRESSION IN THE EUSOCIAL NAKED MOLE-RAT BRAIN 
Hormones and behavior  2008;54(2):278-285.
Naked mole-rats (Heterocephalus glaber) are eusocial rodents that live in large subterranean colonies including a single breeding female and 1-3 breeding males; all other members of the colony, known as subordinates, are reproductively suppressed. We recently found that naked mole-rats lack many of the sex differences in the brain and spinal cord commonly found in other rodents. Instead, neural morphology is influenced by breeding status, such that breeders, regardless of sex, have more neurons than subordinates in the ventromedial nucleus of the hypothalamus (VMH), and larger overall volumes of the bed nucleus of the stria terminalis (BST), paraventricular nucleus (PVN) and medial amygdala (MeA). To begin to understand how breeding status influences brain morphology, we examined the distribution of androgen receptor (AR) immunoreactivity in gonadally intact breeders and subordinates of both sexes. All animals had AR+ nuclei in many of the same regions positive for AR in other mammals, including the VMH, BST, PVN, MeA, and the ventral portion of the premammillary nucleus (PMv). We also observed diffuse labeling throughout the pre-optic area demonstrating that distribution of the AR protein in presumptive reproductive brain nuclei is well-conserved, even in a species that exhibits remarkably little sexual dimorphism. In contrast to other rodents, however, naked mole-rats lacked AR+ nuclei in the suprachiasmatic nucleus and hippocampus. Males had more AR+ nuclei in the MeA, VMH, and PMv than did females. Surprisingly, breeders had significantly fewer AR+ nuclei than subordinates in all brain regions examined (VMH, BST, PVN, MeA, and PMv). Thus, social status is strongly correlated with AR immunoreactivity in this eusocial species.
doi:10.1016/j.yhbeh.2008.03.010
PMCID: PMC2630401  PMID: 18455726
androgen receptor; bed nucleus of the stria terminalis; medial amygdala; naked mole-rat; paraventricular nucleus; plasticity; premammillary nucleus; sex difference; social status; testosterone; ventromedial nucleus of the hypothalamus

Results 1-6 (6)